Transcriptomic Architecture of Reproductive Plasticity
Summary and Keywords
Several species show diversity in reproductive patterns that result from phenotypic plasticity. This reproductive plasticity is found for example in mate choice, parental care, reproduction suppression, reproductive tactics, sex role and sex reversal. Studying the genome-wide changes in transcription that are associated with these plastic phenotypes will help answer several questions, including those regarding which genes are expressed and where they are expressed when an individual is faced with a reproductive choice, as well as those regarding whether males and females have the same brain genomic signature when they express the same behaviors, or if they activate sex-specific molecular pathways to output similar behavioral responses. The comparative approach of studying transcription in a wide array of species allows us to uncover genes, pathways, and biological functions that are repeatedly co-opted (“genetic toolkit”) as well as those that are unique to a particular system (“genomic signature”). Additionally, by quantifying the transcriptome, a labile trait, using time series has the potential to uncover the causes and consequences of expressing one plastic phenotype or another. There are of course gaps in our knowledge of reproductive plasticity, but no shortage of possibilities for future directions.
An individual’s fitness depends on the transmission of its genotype to the next generation. For most animal species, sexual reproduction is thus the pivotal event of an individual’s life and surviving to this moment is a necessary goal. Sexual reproduction involves gaining access to the opposite sex to combine gametes. Mating opportunities and fertilization of gametes represent resources over which individuals compete for, or select more or “better” quality of this resource. As is the case for any resource, we expect animals to adjust in ways that enhance reproductive success (Williams, 1966). Because of these adjustments, reproductive behavior is not as set as we often portray it. Both intersexual and intrasexual selective pressures, along with ecological pressures, have led to the evolution of various reproductive phenotypes (i.e., an animal’s observable traits related to reproduction) to maximize transmission of an individual’s genotype to the next generation.
This diversity in reproductive phenotypes within a species can result from genetic polymorphisms or from phenotypic plasticity (when one genotype can result in more than one phenotype depending on environmental conditions). In many cases, selection has led to the evolution of divergent reproductive phenotypes based on a genetic polymorphism, referred to as alternative “fixed” reproductive strategies (Gross, 1996).
For example, in the ruff, a bird from Eurasia, males can either be territorial, satellite (remain around another’s territory), or fader (mimic females), and these differences in reproductive behavior and reproductive success are the result of genetic differences caused by a chromosomal inversion (Kupper et al., 2016; Lamichhaney et al., 2016). However, in other species, the various reproductive phenotypes, though equally dramatic, are not necessarily fixed from birth. In many cases, the development of an individual’s reproductive phenotype actually depends on internal and external conditions faced early in life or just before the reproductive period.
In these cases of phenotypic plasticity, the reproductive strategy of a species encompasses all the possible phenotypes one individual can take, and each phenotype is termed a tactic. For example, two tactics are present within the reproductive strategy of horned beetles. Based on body condition earlier in development, some male horned beetles grow large weapon structures used to fight off competing males, while other genetically equivalent males from the same population remain small and dig different burrows to sneak access to the females below ground. In these instances, both reproductive tactics allow access to gametes of the opposite sex for fertilization. Knowing more about how these plastic phenotypes arise from a mechanistic point of view will help us to better understand several aspects of sexual reproduction in animals. This will inform us, among other things, on which pathways are the target of modulation by the early environment when it affects development to lead to drastically divergent phenotypes, which pathways are directly associated with reproductive behavior independently of gonadal sex, to what extent these plastic phenotypes could be the precursor to evolutionary divergence, and how they have themselves evolved (see Figure 1).
Here, our goal is to present a picture of the field of reproductive phenotypic plasticity and to highlight the available knowledge on the transcriptomic architecture of these plastic reproductive phenotypes. To do so, we use examples found in a wide range of organisms to emphasize the breadth of approaches and models available to address questions about the underlying mechanisms of reproductive plasticity and the different timescales implicated (see Figure 1 for an outline). We argue that studying reproductive behavior in mammals, but also in fish and insects among others, provides clues to the origin of reproductive plasticity at the proximate (developmental, mechanistic) and ultimate (evolutionary) level. With this work, we aim to present an overview of the types of plastic phenotypes that have been most studied, to identify patterns that have been revealed, and to suggest areas for further inquiry.
Knowing about proximal mechanisms (see “What are proximal mechanisms” for a definition and examples) is useful to address several topics. On a short timescale, an individual must react to a challenge or an opportunity, which is termed activational plasticity or flexibility (O’Connell & Hofmann, 2011; Snell-Rood, 2013). Uncovering how this flexibility is orchestrated at the genomic level on this fairly rapid timescale is an essential step toward understanding how the early environment modulates this genomic response, and ultimately how the presence of these different plastic phenotypes can provide targets of selection that may allow divergent behavioral phenotypes to evolve within a species (e.g., Nyman, Fischer, Aubin-Horth, & Taborsky, 2017; reviewed in Snell-Rood, 2013). Here, we focus on systems that have been used to address this fairly rapid timescale of reproductive plasticity: mate choice. Studying this flexible response from a mechanistic approach includes quantifying and locating gene expression changes associated with the behavioral response of an individual to various opportunities for mating in a social context (Cummings, 2015).
Another long-standing question in the study of reproductive behavior concerns the biological makeup of a female and male brain, and ultimately, an even more basic question: is there even a female and a male brain? This overarching goal requires systems in which we are able to test for the presence of a signature pattern of gene expression related to reproductive role and thus to separate the mechanisms related to building gonads from those related to the expression of behavior. Here, we discuss two forms of reproductive investment that allow us to gather information to answer this question: parental care and reproductive suppression. Studying parental care allows us to test whether individual maternal and paternal care are homologous at the behavioral and the molecular level, and how biparental behavior affects the brain of each sex. It also allows us to ask if the different levels of parental care provided by an individual are reflected by different levels of gene expression and to what extent the neural transcriptome reflects the behavioral phenotype. Studying reproductive suppression, an example of plastic allocation of energy where some individuals engage in reproduction while others in the same population do not, allows us to study how the brain of a single sex is plastically modulated in association with reproductive behavior.
Additional systems to address these questions are species where we find alternative reproductive tactics. These systems allow us to differentiate the biological mechanisms that are associated with reproducing as a male (male gonads) versus those that are associated with outward expression of typically male behaviors, those that are associated with typically female behaviors (in cases where one of the alternative male morphs mimic the females), or that are associated with the unique behavioral repertoire of an alternate male tactic. Because of the wide range of species in which alternative reproductive tactics have been studied, a comparative approach (see section “In which systems should we study proximal mechanisms” for a definition) enriches our understanding. Finally, questions about the underlying mechanisms leading to female and male brains can also be approached using plastic sex change, which includes transitional phenotypes between a “fully” female and a “fully” male endpoint such that the biological mechanisms related to behavior can in part be differentiated from the biological mechanisms related to a particular gonad type. Sampling at different times following the environmental signal that lead to a plastic response is one way we can go beyond correlation between transcription and organismic phenotype and get at causal mechanisms (see section “When should we study proximal mechanisms?”for details and further references).
Mate choice, either by males or by females, creates a strong selective force that can favor one tactic or another in the opposite sex (Alonzo, 2008). Classically, mate choice has been viewed as an innate or genetic preference, reflecting adaptations to past selective pressures. Different models of genetically based mate choice explain these selective pressures as direct benefits, sensory biases, or indirect genetic benefits (Andersson & Simmons, 2006).
However, more recently, plasticity in mate choice has been shown to impact the evolution of reproductive phenotypes (Varela, Matos, & Schlupp, 2018). On a very short timescale, individuals make choices when faced with a potential mate and this plastic reproductive phenotype can be studied at the mechanistic level in the brain (O’Connell & Hofmann, 2011). Females are often the sex choosing their mate (Andersson, 1994) and several instances of plasticity in female mate choice that depend on immediate external context or internal conditions have been studied (reviewed in Johnson & Brockman, 2012), including mate choice copying and contingency choice. For example, in the sex changing blue-headed wrasse, smaller females choose between the two male reproductive tactics, pair or group spawning, based in part on location, while larger females engage primarily in pair spawning (Warner, 1984). Thus, both internal context (size) and external context (location) influence the choice a female will make. The degree to which female choice versus male coercion influences the mating decision and reproductive success depends on the female’s resistance to coercion, which can vary with age, size, condition, experience, environmental factors, and population density (water strider: Lauer, Sih, & Krupa, 1996; Alonzo, 2008; guppies: Magellan & Magurran, 2006; Farr, 1980). Thus, the strength of female choice as a selective pressure on male form and reproductive behavior will vary. Therefore, by first understanding the mechanistic basis for female choice we can begin to move toward a better understanding of the mechanisms that underlie its plasticity and eventually their impact on the evolution of reproductive behaviors.
The song sparrow presents a promising system for the mechanistic study of mate choice. Here, females change the strength of their song preferences according to the relative attractiveness of song that it recently experienced, such that following a previously attractive experience the female’s song quality threshold for approaching a male will increase (Sockman & Lyons, 2017). These behavioral changes are orchestrated by changes in monoamine signaling, and these differences at the neurochemical level likely result from changes in gene expression level (Lyons & Sockman, 2017).
Studies at the transcriptomic level of female mate choice are still rare, and while a consensus has not emerged from these results, they underscore the need to localize the changes in the brain at this biological level before fully addressing the molecular mechanisms that produce plasticity in this behavior. The initial molecular studies of female mate choice logically used a single gene approach, focusing on immediate early genes already shown to be good markers of neural activity, in specific brain regions and under various behavioral paradigms. While the commonly used immediate early genes differ between study organisms, they can be used in isolation (e.g., ZENK, female starling: Sockman, Gentner, & Ball, 2002; egr-1, swordtail: Wong, Ramsey, &Cummings, 2012) to identify active brain regions, or in conjunction with neuron-type specific markers (e.g., egr-1 and fos with GnRH, Tungara frogs: Burmeister, Mangiamele, & Lebonville, 2008; Burmeister & Wilczynski, 2005) to identify the specific neuron populations that are involved.
Research in this area went on to combine this immediate early gene approach with transcriptomics by studying how the female brain responds to different social cues, such as a preferred male, a non-preferred male, and a non-sexual social cue using a conspecific female (swordtail fish: Cummings et al., 2008). In order to study the underlying mechanisms of variation in mate preference with the goal of understanding its evolution, one approach is to study the brain gene expression response after exposure to another individual in several genetic backgrounds known to differ in their response to social stimuli.
A study on two selection lines of females that differ in their tendency to prefer a mate (one line shows high preference for an attractive male, while the other shows no preference), allows one to study the differential transcriptomic response of a female to an attractive male versus a non-attractive male (and to a female as a social “control” situation) (Bloch et al., 2018). More importantly, it made it possible to determine how this differential response diverges in the two selection lines that exhibit different behavioral output to these social contexts. The expression profiles of females from the two lines were very different and the two studied brain regions associated with two crucial steps of mate preference leading to reproduction, the sensory input step (optic tectum) and the decision-making step (dorsal and ventral telencephalon including the POA + olfactory bulbs), were activated differently (Bloch et al., 2018). From this study and others, we can draw the conclusion that within and between species, distinct social/reproductive contexts evoke specific behavioral responses in female poeciliids that are paralleled by changes in gene expression level for genes related to nonapeptides, hormone synthesis and synaptic plasticity (Cummings et al., 2008; Lynch, Ramsey, & Cummings, 2012, reviewed in Cummings, 2015; Ramsey, Maginnis, Wong, Brock, & Cummings 2012; Wong & Cummings, 2014). The generalizability of neural gene expression studies across species with similar behaviors is bolstered by the identification of conserved gene expression patterns across brain regions of closely related cichlid species (Derycke et al., 2018).
While the aforementioned studies, as well as the bulk of mechanistic studies related to plasticity of mate choice, do address plasticity on this relatively rapid timescale of recent experience and social context, early social learning and imprinting can also mediate mate choice in later life. While classically studied at a behavioral level, sexual imprinting is known to occur in a broad range of taxa with the potential to impact the evolution of a population (Bateson, 1978; Grant & Grant, 1997; Verzijden et al., 2012). This form of plasticity in mate choice occurs on a longer timescale that is more often considered in mechanistic studies of alternative reproductive tactics, though a few studies have begun to address transcriptomic adjustments of early life conditions on later mate choice behavior (e.g., Cui, Delclos, Schumer, &Rosenthal, 2017; see Rittschof & Hughes, 2018, for a review of early environmental effects on plasticity in general). This study finds that adult olfactory preference for species recognition in swordtail females (Xiphophorus malinche) is affected by early experience of adult olfactory signals and suggests that adjustments in vomeronasal receptor gene expression may play an important role in reproductive isolation between species in the form of plasticity mediated through sexual imprinting (Cui et al., 2017). Uncovering which biological functions are affected by these differences in early environment linked to a different plastic response later in life will help define how these mate choice changes are mediated, how they could eventually evolve, or be affected by human-induced environmental perturbations that affect these molecular mechanisms by acting as information disrupters (Lürling & Scheffer, 2007).
The amount of energy and time that an individual invests in reproduction can be affected by the external and internal environment, such that there can be variation between individuals within a population but also within an individual over its lifetime. This variation reflects the trade-off between investing in certain life history traits versus others: current and future reproduction, growth, and survival (Stearns, 1992). This plasticity in reproductive investment affects both the individual and the population dynamic. While the associated trade-offs have been studied for decades, the mechanisms have traditionally been viewed as a black box (Stearns & Magwene, 2003). Here we focus on two types of reproductive investment plasticity: parental care and reproductive suppression, with special discussion of eusocial insects.
Plastic variation in parental care within a population has been shown in several species of mammals (reviewed in Kundakovic & Champagne, 2015). For example, it has been shown in rodents that the quantity of maternal care a female offspring receives affects its own later expression of maternal care (Champagne & Meaney, 2007). This plasticity in parental care has been extremely well dissected at the neuroendocrine level to implicate epigenetic regulation of components of the stress axis in the hypothalamus of the caregiving mother (Champagne & Meaney, 2007).
For a very different example in which the two sexes can be compared, burying beetles represent an interesting case of plasticity in parental care level: either parent alone can provide sufficient uniparental care if one parent abandons the brood, but parents also naturally remain paired to provide biparental care. This system allows us to ask whether individual maternal and paternal care are behaviorally and molecularly equivalent, and whether individuals that provide different levels of care show gene expression differences when solitary versus paired (Parker et al., 2015). Interestingly, in a laboratory setting, offspring survival and time to dispersal were not dependent on the type of parental care provided. The brain transcriptome results from these studies show a strong correlation between gene expression regulation and the transition from non-parental to parenting, but biparental males show fewer differentially expressed genes and lower fold change in expression level than uniparental males or either parental female phenotype (Parker et al., 2015).
These molecular data suggest that males show a highly flexible parenting strategy and only fully express the gene expression modules associated with parenting when the female abandons the brood, leaving the male to attend the young alone. Using the set of genes that were differentially expressed between parents and non-parents in this beetle species as a transcriptome signature of parenting (from Parker et al., 2015), it was shown that many of these transcripts were also differentially expressed between low and high-provisioning parents for both sexes (Benowitz, McKinney, Cunningham, & Moore, 2017). The authors claim that these data suggest that variation in parenting phenotypes are obtained by further modulation of the same molecular mechanisms that underlie the initiation of that behavior. Studying other biparental care species that express plastic phenotypes will further provide information on whether maternal and paternal care are homologous at the behavioral and the molecular level, and thus separate the mechanisms related to building gonads from those related to the expression of offspring care.
Another example of plastic variation in parental care is found in species where individuals parasitize the brood of another individual. Roughly 1% of bird species are brood parasitic, which is an evolutionary derived strategy in which males and females display no parental care (Winfree, 1999). While previously considered rare relative to obligate interspecific brood parasitism (Payne, 1977), facultative intraspecific brood parasitism, a reproductive tactic in which a female lays some of her eggs in the nests of other conspecific females, is now known to exist in over 200 species of birds (Yom-Tov, 2008). For some species, this behavior is highly plastic, such as the ruddy duck, in which females lay parasitic eggs whenever the opportunity arises (Reichart, Anderholm, Munoz-Fuentes, & Webster, 2010), while in others such as starlings, the females parasitize other starlings or raise their own young but do not do both simultaneously, only using this parasitic tactic to increase its reproductive success when it is unable to find a suitable nest site (Sandell & Diemer, 1999).
These plastic phenotypes have not been studied at the gene expression level but doing so would allow us to use a comparative approach by studying the genes that have been found to have evolved different expression levels between obligate parasitic species and non-parasitic species to determine if they are also involved in plastic divergence of reproductive tactics in facultative parasitic species. For example, Lynch et al. (2019) compared two brood parasitic species, the brown-headed and the bronzed cowbirds, with a non-parasitic one, the red-winged blackbird. Rather than finding the predicted reduced expression of parental-related genes in the obligate brood parasitic species, that study uncovered a general retention of juvenile (neotenic) gene expression in the preoptic area. These neurogenomic results are consistent with the observed morphological neoteny in plumage color and skull formation for the parasitic species. While previous studies of brood parasitism have focused on the adaptive value of the behavior to determine why these behaviors evolved, taking a mechanistic approach will also shed light on how these behaviors have evolved. Intra- and interspecific brood parasitism is also present in many fishes (Wisenden, 1999) and exists as an alternative tactic to crevice spawning (Yamane, Watanabe, & Nagata, 2009). It is also found in amphibians (Harris, Hames, Knight, Carreno, & Vess, 1995) and various species of insects (Brockmann, 1993; Tallamy, 2005). While the plasticity of these behaviors has largely been studied at the environmental and behavioral level, they represent a rich area for future mechanistic study.
In several species, individuals that can reproduce show no sexual behavior or gonadal development. This reproductive suppression can be permanent or related to the current dominance status. Studying this type of reproductive plasticity allows us to study how the brain of a single sex is plastically modulated in association with reproductive behavior. We learn about the degree to which the brain transcriptome reflects the behaviors that an individual engages in versus the behaviors in which they are capable of engaging. In many cases, these systems also give us the opportunity to manipulate the social environment and “release” the reproductive suppression. While many studies have taken advantage of this ability to manipulate the system and produce the endpoint phenotypes in a more controlled setting, only a few have fully capitalized on it to produce a time course study and investigate cause and effect as well as transitional states (see “In Which Systems Should We Study Proximal Mechanisms?”). Finally, by studying reproductive suppression, we can get at some of the mechanisms and use them to pursue a candidate gene approach, to see if the same regulators and targets are “re-used” on an evolutionary timescale.
In the African cichlid Astatotilapia burtoni, males switch between two states on a timescale of days to weeks. Dominant males are brightly colored, territorial, and reproductive, while subordinate males are drab, non-territorial, and sexually inactive (reproductively suppressed) (Fernald & Hirata, 1977). These fish have been used as a model system to study neural and endocrine mechanisms of a plastic reproductive phenotype on a relatively rapid timescale. Genomic level studies have focused on the endpoint phenotypes (Renn, Aubin-Horth, & Hofmann, 2008) and have addressed how the gene expression differences associated with male status can be further subdivided by comparing the patterns to gene expression in reproductive females, in order to differentiate those genes associated with reproduction from those associated with behavior.
This approach showed that some genes (including both candidate neuroendocrine pathways and novel functional categories) were specifically differentially expressed in association with dominance and territoriality, while others were specifically expressed according to reproductive status. Interestingly, manipulating the social environment of females by placing them in an all-female population can induce an unnaturally aggressive female phenotype with male-like coloration and male-biased hormone levels (Renn, Fraser, Aubin-Horth, Trainor, & Hofmann, 2012). The neural gene expression profile of these male-like females could be compared to that of males to identify a gene module associated with the plastic expression of a territorial aggressive phenotype independent of gonadal phenotype (Renn, O’Rourke, Aubin-Horth, Fraser, & Hofmann, 2016). This system also presents the opportunity to experimentally manipulate male status by changing the social environment (Francis, Soma, & Fernald, 1993; White, Nguyen, & Fernald, 2002), which could be used to produce a time course analysis of gene expression, which has been done using a candidate gene approach in males (Huffman, Hinz, Wojcik, Aubin-Horth, & Hofmann, 2015) and showed that some genes are indeed differentially expressed only in the transient state, but has not yet been attempted on a genomic scale.
In the cooperatively breeding African cichlid fish Neolamprologus pulcher, dominant males and females are reproductively active, while most subordinate males and females are reproductively suppressed. The neural gene expression profile of dominant females is similar to that of males (both dominant and subordinate), suggesting that dominant breeder females are masculinized at the molecular and hormonal level, while being able at the same time to show female appropriate reproductive behavior and physiology (Aubin-Horth, Desjardins, Martei, Balshine, & Hofmann, 2007). This result suggests a modular organization of molecular and endocrine functions.
A similar picture emerges in birds, with the white-browed sparrow weaver (Plocepasser mahali). This cooperatively breeding bird species also has groups consisting of a dominant breeding pair and male and female subordinates. While all male and female group members sing duet and chorus songs, only dominant males sing a solo song at dawn. Important brain nuclei of the song circuit (HVC and RA) are 30% larger in dominant than in subordinate males or females of either status, while the expression levels (as assayed by in situ hybridization) of androgen and oestrogen receptors as well as synaptic proteins (SNAP-25 and synaptoporin) are lower in dominant males (Voigt & Gahr, 2011; Voigt, Leitner, & Gahr, 2007). While some sex differences in morphology and cell number were detected, these gene expression results are consistent with patterns described for dominant and subordinate fish in which the subordinate males more closely resemble the dominant females (Aubin-Horth et al., 2007).
Hormone studies in a wide range of cooperatively breeding bird species demonstrate the need to take a broad comparative approach that accounts for ecology. For example, in many cooperatively breeding species, dominant males have elevated testosterone levels relative to helper subordinate males, suggesting that testosterone is related to social status; however, testosterone does not differ between breeder and helper males in other species (Pikus, Guindre-Parker, & Rubenstein, 2018). Here, transcriptomic studies could help uncover the mechanisms by which testosterone levels differ between male breeding roles or across social status in some cooperatively breeding species but not others.
Reproductive suppression is also present in mammals and lineage-specific mechanisms are also found in this vertebrate group. Both the naked mole-rat and the Damaraland mole-rat exhibit an extreme skew in lifetime reproductive success, with breeding restricted to a single female and one or two males, resulting in a eusocial system more commonly associated with insects. Unlike strict eusocial insect caste systems, the reproductive suppression is socially maintained and can be reversed should the dominant breeding individuals be removed. However, 90% of the individuals in a colony will never reproduce under this extreme reproductive suppression.
While both sexes are physiologically inhibited from reproducing in the naked mole-rat, only the females are physiologically suppressed in Damaraland mole-rats, while the males are simply behaviorally suppressed. Unlike naked mole-rats, non-reproductive male Damaraland mole-rats maintain a functional hypothalamic-pituitary-gonadal axis (HPG axis) and their relative testicular mass and testosterone titers do not differ from that of reproductive males (Bennett, 1994; Voigt, Leitner, & Bennett, 2016). Similarly, where female naked mole-rats exhibit prepubescent ovaries (Mulugeta et al., 2017), non-reproductive female Damaraland mole-rats have fully developed ovaries that fail to ovulate (Molteno, Kalló, Bennett, King, & Coen, 2004). Therefore, these convergently evolved systems of reproductive suppression differ with regard to the underlying mechanisms.
To a large extent, research in these systems has followed a candidate gene approach to address the underlying molecular mechanisms. Relative to breeders, the non-reproductive male Damaraland mole-rats have decreased expression of androgen receptors in most brain regions (Voigt et al., 2016; Voigt, Gahr, Leitner, Lutermann, & Bennett, 2014), but particularly in pathways that relay olfactory information related to reproduction (e.g., the bed nucleus of the stria terminalis (BSTp) and the medial amygdala (MeA)) (Simerly, Young, Capozza, & Swanson, 1989). Like breeders, non-breeders released from reproductive suppression show increased androgen receptor and estrogen receptor α expression and reduced aromatase expression, thus implicating these steroid hormone related changes as functional mechanisms for the behavioral reproductive suppression.
A recent transcriptomic study in naked mole-rats revealed an increase in dopamine metabolism activity in breeders that could be localized to a brain region known to suppress prolactin expression. As predicted by those gene expression results, plasma concentrations of this neurohormone (implicated in increased parental care and reduced reproduction) was elevated in the non-reproductive animals (Mulugeta et al., 2017). When investigated in Damaraland mole-rats, apart from the breeding queen, prolactin was not detectable in most individuals, which might explain the lack of gonadal suppression in non-reproductive individuals of this species. Again, these results reveal a lack of evolutionary convergence in the proximate control of overtly similar behavioral phenotypes in these mole-rats (Bennett et al., 2018). These studies show the advantage of using complementary transcriptomic and candidate gene approaches in a comparative context.
Due to the dramatic diversity of reproductive phenotypes across Hymenoptera, they have long been studied to understand the evolution of eusociality (Oster & Wilson, 1978). Transcriptome studies across hymenoptera systems are perhaps the best example of applying a comparative approach not only to understand the mechanisms that underlie plasticity in a single species, but also to understand how the social systems that involve reproductive plasticity evolve over time.
Castes of morphologically distinct reproductive and non-reproductive phenotypes share genomic content and are produced through differential expression of shared genes (Smith, Toth, Suarez, & Robinson, 2008). Worker sterility is a defining characteristic in the caste-based eusocial species common among hymenoptera, but there also exist a number of “primitively” eusocial insect species in which workers retain the ability to reproduce. Transcriptome studies conducted on primitively eusocial terrestrial insects can be used to test competing theories regarding the evolution of true obligate, or advanced eusociality (Shell & Rehan, 2018) by outlining common patterns and singularities, in order to define which types of genes and pathways are used to build a eusocial species.
Although the well-resolved phylogenies that are now available suggest that social structure in these species may evolve along a non-linear path, these studies provide a foundation for ongoing transcriptomic studies (reviewed in Rehan & Toth, 2015). For example, in the paper wasp, many females are capable of reproducing during initial nest construction and colony formation, competing for the reproductively dominant position in the established colony where caste-like phenotypes predominate (e.g., Mora-Kepfer, 2011; Zanette & Field, 2011). Similarly, in carpenter bees, the established dominant queen female can rear worker-like offspring that aid in both brood care and feeding while ovary development is inhibited. In both cases these workers retain capacity for reproductive behavior upon removal of the dominant reproductive nest mate and the caste differences in behavior are determined through differential gene expression throughout adulthood. In the primitively eusocial bumblebees (Bombus terrestris), brain gene expression in foundresses, who engage in both care and reproduction, is more similar to that of an established queen, who engages only in reproduction, rather than to that of workers who only provide care (Harrison, Hammond, &Mallon, 2015; Woodard, Bloch, Band, & Robinson, 2014).
Those results suggest that brain gene expression more closely reflects reproductive behavior than care behavior. However, in paper wasps, the brain gene expression pattern of the foundress is more similar to that of workers that engage in offspring care, than to the established queens that engage only in reproductive behavior (Toth et al., 2007). This suggests that in this species, care is a driving factor in brain gene expression. Care similarly represents a predominant signal in the brain gene expression of carpenter bees (Rehan, Berens, & Toth, 2014), where the gene expression pattern of worker-like daughters is more similar to that of post-reproductive females that engage in care. Comparative analyses show that the gene expression pattern associated with plastic queen status in paper wasps is different from that associated with the outwardly similar queen phenotype of the caste system in bees, which includes genes related to pheromone processing (Toth et al., 2014).
Interestingly, for paper wasps, the expression pattern includes genes more likely to be involved in aggression in other insects (bees: Alaux et al., 2009; flies: Edwards, Rollmann, Morgan, & Mackay, 2006), and even a mammal (mice: Gammie et al., 2007), suggesting that genes involved in social regulation of reproduction in paper wasps may have conserved functions associated with aggression in insects and other taxa. These and other studies have supported the idea of a “behavioral genetic toolkit,” particularly with regard to metabolic pathway and molecular functions that are relatively well conserved across distant lineages (e.g., Bloch & Grozinger, 2011; Rehan et al., 2014; Rittschof & Robinson, 2016; Saul et al., 2018).
In the absence of expression studies, direct genome comparisons are also used to address the mechanisms underlying the evolution of distinct eusocial castes, for example by identifying conserved genes and regulatory elements across primitively eusocial bumble bees and paper wasps contrasted with highly eusocial honeybees (A. mellifera) (Sadd et al., 2015). These genomic comparisons show that while overlap exists, there are specific biological functions that seem to have evolved along with eusociality. Interestingly, the majority of the differentially expressed genes in paper wasps are novel, clade specific genes, having no or little significant homology with described sequences (Ferreira et al., 2013) even though similar pathways are associated with caste in primitively eusocial paper wasps compared to highly eusocial honey bees. In an attempt to resolve the apparent conflict between evidence in support of a genomic toolkit and evidence in support of the involvement of novel or positively selected lineage-specific genes in constructing eusocial phenotypes, Shell and Rehan (2018) suggest that eusociality can evolve from multiple antecedent gene expression patterns associated with plasticity, yet the composition of genes and further evolution of those networks is constrained as species approach advanced forms of social complexity.
Alternative Reproductive Tactics
There is more than one way to be male, as some males monopolize assets that increase their chances of reproducing, as seen in males that defend a territory or the female directly, while others gain access to the opposite sex without investing in the control of resources. These two types of males may be more different in their behavior and appearance than males and females. When these two (or more) types of males are due to a genetic polymorphism, the two types of males are said to be exhibiting alternative strategies. These strategies are often the result of sexual and natural selection. When these two types of males are not due to a genetic polymorphism between the males, and instead a single male genome is capable of producing either phenotype as an adult, or even switching between them, these types are referred to as alternative reproductive tactics (ARTs). The literature on alternative reproductive tactics is strongly biased towards males, although the extent to which this is because ARTs actually occur more frequently in males than in females or because there is a study bias is not clear (Johnson & Brockmann, 2012).
Some sources contend that it is not helpful to categorize alternative strategies (two genetic programs) and alternative tactics (a single genetic program with alternative outputs) as two different types of reproductive plasticity (Stamps, 2015; Taborsky, Oliveira, & Brockmann, 2008). We argue that, when it is possible to know, this distinction is important, because only then can we address the greater question about the degree to which phenotypic plasticity (alternative tactics) either buffers against evolutionary diversification (alternative strategies) or contributes to it through processes including genetic accommodation (see West-Eberhard, 2003, for a complete discussion).
Plastic phenotypes considered among ARTs generally include two or more different tactics that are found within one sex, that are both capable of reproduction, and that represent discrete phenotypes rather than a continuum, as is seen in differential parental investment and other forms of plasticity. (Maruska, Butler, & Field, 2018; Taborsky et al., 2008), or the more dramatic plasticity involved in sex change. This type of polyphenic plasticity of reproductive phenotype has been found in several species, including in arthropods (insects: Moczek & Emlen, 1999, horseshoe crab: Brockmann, 2002) and vertebrates (amphibians: Arak, 1988; fish: Dodson, Aubin-Horth, Theriault, & Paez, 2013; Taborsky, 2001).
The expression of one alternative reproductive tactic or another is dependent on an individual’s assessment of internal and/or external conditions within a specific time window. In some cases, this window is early in life and determines how development proceeds, leading to a specific fixed reproductive phenotype and tactic. In other cases, the time of assessment precedes each reproductive event and prepares the individual to express one reproductive phenotype or another in a reversible fashion. This implies that individuals are already diverging in their development much before we can detect the morphological, physiological and behavioral changes associated with the reproductive path they have initiated. This adaptive reproductive plasticity is predicted to allow an individual to increase its fitness in fluctuating environments by matching its reproductive tactic to the surrounding or predicted conditions.
For example, a male horned beetle of large size is able to access reproduction using a competitive tactic, fighting for access with a weapon in the form of a horn, while the same fighting tactic would result in very low fitness for a smaller male with lower condition and no weapon (Emberts, St Mary, Herrington, & Miller, 2018). The male’s own condition is the environmental factor to which the male’s tactic is matched and this condition is environmentally-determined by nutrition provisioned by its mother (Emlen, 1996). Conditions above a certain threshold during the time window preceding the switch causes commitment to one developmental pathway or another. Due to the reproductive plasticity in this species, a small-sized male (who received less food provisioning from its mother and did not pass the size threshold) instead develops an alternative reproductive tactic and sneaks to access reproduction, thus potentially gaining higher fitness than if it had tried to fight for access to females. The fitness advantage of being able to develop into one type or another is clear when we compare it to a fictional fixed reproductive strategy: if a male expresses the same fighting behavior as its father independent of its size, but the fitness gained by this phenotype is strongly affected by the male’s size, this would lead to little or no reproduction for the male when its condition is sub-optimal for gaining reproduction with that strategy. This expected relationship between condition (here, size) and fitness is central to the evolution of reproductive plasticity when the condition of an individual is environment-dependent.
Systems that separate the behavioral phenotype associated with reproduction, such as aggressiveness in males, from the actual development and use of gonads to reproduce provide a powerful tool to study the mechanisms of behavior separately from the mechanisms of reproduction per se. We can ask whether the divergent morphs of the same sex are mechanistically more similar to each other or whether the overt behavioral similarities, for example between a female and a female-mimicking male, are orchestrated by similar gene expression regardless of gonadal sex.
ARTS in Fish
There are at least 25,000 species of fish, making them the largest group of vertebrates and a valuable model to understand the molecular basis of ARTs. Accordingly, most of the transcriptomic studies of this type of reproductive plasticity have been done in fish, and the number of different species studied in this group makes it possible to draw a general portrait of the male and female brain according to behavior rather than gonadal sex. Fish ARTs often include two or three types of males that compete for access to females using different tactics. In summary, it has been demonstrated in several species that in the brain, more genes are differentially expressed between the different male phenotypes than between males and females, suggesting that during the reproductive period, the plastic reproductive tactic is a stronger factor of differential gene expression in the brain than is sexual dimorphism.
The first brain transcriptomics work on male ARTs in any vertebrate was done on the well-described Atlantic salmon system. In this species, males are either large individuals returning from the sea that fight to control access to females, or small individuals that have not left their freshwater birthplace and that furtively access fertilization opportunities by sneaking close to the reproductive pair during a fertilization event (Garcia de Leaniz et al., 2007). Quantifying brain transcription differences early in life between males that mature early and become sneakers, males of the same age that stay immature and are on the developmental path to become large fighting males, and females, shows that the two types of males are more divergent from each other than mature sneaker males are from females of the same age (Aubin-Horth et al., 2005a). Transcriptomics show that differences between the two male tactics remain, regardless of whether males are reared in natural stream conditions or laboratory ones (Aubin-Horth et al., 2005b), and that mature sneaker males show physiological trade-offs both at the gene expression and life history level between reproduction and the potential to migrate at sea later (Aubin-Horth, Letcher, & Hofmann, 2009).
In black-faced blennies (Tripterygion delaisi), territorial and sneaker males are also more different from each other than from females (Schunter, Vollmer, Macpherson, & Pascual, 2014). In the peacock blenny (Salaria pavo), the females rather than the males are the courting sex. Despite this sex-role reversal in courtship, it is still the males that display an alternative reproductive tactic with older, larger males holding nests while younger, smaller males sneak copulations. In this case, it is the sneaker males that exhibit the most divergent neural gene expression patterns while nest-holding males and females are more similar to each other (Cardoso, Goncalves, Goesmann, Canario, & Oliveira, 2018). Interestingly, in the plainfin midshipman (Porichthys notatus), there are two environmentally determined morphological types of males, a large and a small type (Type I and II), and within the large morph, some individuals behave as courting and nesting males and others as sneakers (cuckolders), while all small males are sneakers. Studying transcription specifically in the pre-optic area (POA), it was shown that being a sneaker/cuckolder had more influence on gene expression than which size morph a male expressed (Tripp, Feng, & Bass, 2018). All of these studies point to a very strong association between behavior and brain gene expression.
The ocellated wrasse, Symphodus ocellatus, offers an interesting example of male ARTs since males exhibit one of three stable tactics (sneaker, satellite, and nesting) within a season, but transition across seasons such that some males breed as sneakers in the first year and as satellite males in the second, while others switch from being satellites or non-reproductive males to nesting in their second reproductive season (Alonzo, 2000). Brain transcriptomes of satellites and females are most similar to each other and intermediate to nesting and sneaker males. While sneaker males show the greatest number of differentially expressed genes, the nest males show the greatest magnitude of expression level variation (Stiver, Harris, Townsend, Hofmann, & Alonzo, 2015).
Using a brain region-specific and candidate gene approach focused on the expression of hormone receptors, similar to results in mole-rats (Voigt et al., 2014, 2016), suggested that anatomical localization of specific receptor expression may underlie some of the phenotypic differences. Indeed, satellite and nesting males were shown to have higher expression of androgen, oestrogen, mineralocorticoid and glucocorticoid receptors than females and sneakers across several brain regions (Nugent, Stiver, Alonzo, & Hofmann, 2016). In bluegill sunfish (Lepomis macrochirus), reproductive phenotypes also include parental, satellite, and sneaker males. Here again, larger differences are found between the different male types than between males and females (Partridge, MacManes, Knapp, & Neff, 2016). Interestingly, sneaker males in bluegill sunfish show increased expression of genes with biological functions related to spatial working memory, a process also implicated in the ARTs of voles (see Ophir, 2017). This differential expression of genes related to neuroplasticity had also been found in sneaker males of Atlantic salmon (Aubin-Horth et al., 2005a), sailfin mollies (Fraser, Janowitz, Thairu, Travis, & Hughes, 2014) and bluehead wrasses (Todd et al., 2018).
These studies point to the possibility of drawing inferences about the evolution of reproductive plasticity by studying the molecular mechanisms in different species where divergent reproductive tactics have evolved repeatedly. Collectively, these studies have established that sexual selection drove the evolution of divergent gene expression patterns in the brains of males expressing different tactics. Recently, it has been proposed that this is especially true for sex-biased genes (Cardoso et al., 2018; Veltsos, Fang, Cossins, Snook, & Ritchie, 2017). Indeed, using reproductive females and nesting males as examples of the typical male and female transcriptome, classifying the sneaker males’ differentially expressed genes shows that for those genes that showed a sex-bias between nest males and females, the sneakers appeared to be simultaneously feminized (with higher expression of the genes that are female-biased) and demasculinized (with lower expression of the genes that were male-biased) (Cardoso et al., 2018). A number of studies have examined sex differences in gene expression (e.g., mouse: Yang & Shah, 2014, among others) providing large lists of candidate genes with which to test this hypothesis of a shift in the transcriptome toward feminization and demasculinization in the alternative, non-fighting male phenotype. Furthermore, the repeated finding that these “sneaker” males show higher expression of genes related to neuroplasticity offers another hypothesis to test in other vertebrates. In sailfin mollies, for example, variation in male reproductive behavior is both genetically-determined and the result of plasticity, depending on the male (Fraser et al., 2014). In this system, sneaking behavior (whether it results from plasticity or from a genetically-regulated behavioral reproductive morph), but not courting, is associated with upregulation of genes involved in learning and memory. This suggests that sneaking is more cognitively demanding than courtship. In summary, a comparative approach using genomics for hypothesis testing (in addition to the traditional hypothesis generating approach) is within reach, as the growing number of datasets in closely related species or different contexts within a species now allow this.
ARTs in Birds
There are over 200 species of cooperatively breeding birds. While about half of these species nest in nuclear family groups, suggesting the behavior is maintained by kin selection, the others, particularly the obligate cooperative breeders, nest in mixed groups or even groups of primarily non-kin. In either case the behaviors represent a diversity of alternative reproductive phenotypes (Riehl, 2013). In birds, the majority of research on ARTs has been done from an ecological perspective (e.g., Shen, Emlen, Koenig, & Rubenstein, 2017) with few being studied at the level of mechanism. One of these few is the manakins. The cooperative behavior seen among some neotropical manakins (family Pipridae) (Prum, 1994) is restricted to coordinated courtship displays among males. Here, two males display, yet only the dominant alpha will reproduce, while the subordinate beta males forego reproduction for up to five years (e.g., DuVal, 2013). Because males can either initially display as alphas or begin by displaying as betas and then transition, the beta phenotype that later transitions to alpha can be considered an alternative reproductive tactic (DuVal, 2013). Hormone studies in this species reveal increased androgen levels in alpha males compared to beta males, and beta males had similar androgen levels to unpaired adult males. This suggests that plasma testosterone in this species is associated with copulatory behavior in a distinct manner from display behavior (DuVal & Goymann, 2011). Studies at the mechanistic level, conducted with a comparative approach cognizant of ecology and natural history, will be necessary to reveal overarching patterns among birds and further compare and contrast these gene expression patterns with those for bony fishes and other clades.
ARTs in Mammals
The general framework of plastic ARTs has been recently applied to the study of mammal mating systems. In several species, such as in big-horn sheep (Hogg & Forbes, 1997), males that defend reproductive resources are found along with subordinate males that successfully sneak or steal fertilisation (reviewed in Wolff, 2008). In other species, both males and females engage in alternative tactics. For example, one of the species best described at the mechanistic level, the prairie vole, is characterized as socially monogamous, but both males and females engage in alternative reproductive tactics, being either unpaired wanderers or true residents. In males, a subset of residents also engages in extra pair copulations and are referred to as rovers (reviewed in Ophir, 2017). Nonapeptide receptors, like oxytocin receptor (OTR) and vasopressin 1a receptor (V1aR), modulate a variety of functions across taxa, and mediate phenotypic variation within and between species (Kelly & Vitousek, 2017). Inter-species differences in nonapeptide receptor distribution associated with mating strategy (monogamy versus promiscuity; Goodson, 2008; Insel, 2010) suggested the hypothesis that intra-species alternative reproductive tactics might also involve nonapeptide receptor density in regions of the limbic system, which is associated with pair-bonding (Insel et al., 1994; Insel & Shapiro, 1992). Interestingly, the within-species receptor density differences that correlate with alternate male phenotypes (resident versus wanderers) are not found in the limbic system, but rather in areas of the brain normally associated with spatial memory (reviewed in Ophir, 2017), a system also implicated through gene expression studies of ARTs in fish (see Partridge et al., 2016). While some of the intraspecific variation may be due to genetic differences (Okhovat, Berrio, Wallace, Ophir, & Phelps 2015), recent evidence also suggests that social and spatial complexity in early life can influence adult expression level of these important mediators of social behavior (Prounis, Foley, Rehman, & Ophir, 2015; Prounis, Thomas, & Ophir, 2018). Since both reproductive types reproduce, these differences are associated with reproductive behavior variation.
ARTs in Insects
Studying reproductive plasticity involves studying the brain to understand reproductive behavior, but we must keep in mind that these are complex traits also involving physiology and morphology. A model system in the study of complex alternative reproductive phenotypes is that of the dung beetle (Onthophagus taurus), in which males show condition/nutrition dependent alternative reproductive phenotypes with regard to their namesake structure as well as a suite of other morphological and behavioral traits that include mate guarding versus sneaking (Moczek & Emlen, 2000). While female size is also sensitive to nutrition level, they show only a continuum of body size, like females in many other systems of conditional dramatic switch in morphology and behavior. Genome-wide studies in this species have examined sexually dimorphic gene expression in different tissues and concluded that the degree of sex-biased gene expression (number of genes and magnitude of expression difference) correlates with morphological differentiation between the sexes and that increased nutrition further promotes these morphological sex biases. Furthermore, sex-biased genes that are nutrition-dependent are for the most part tissue-specific (Kijimoto et al., 2014; Ledon-rettig & Moczek, 2016).
These dung beetle studies, though focused on morphological rather than behavioral phenotypes, may prove illuminating regarding the specific time window in which the “decision” to take a certain developmental path is made. Indeed, these studies give us information on the mechanisms that initiate condition-dependent reproductive phenotypes and the degree to which these mechanisms are tissue- and sex-specific in their environmental responsiveness. Researchers have taken a candidate gene approach toward the goal of identifying specific regulatory mechanisms focused on the gene doublesex (dsx) which is known to be an important regulator of sexually dimorphic gene expression and phenotypes across metazoans. They were able to show that in the horn beetle, dsx regulates gene expression by acting both as a sex-specific modulator and as a switch regulating the same genes in males and females but in opposite directions (Ledon-Rettig, Zattara, & Moczek, 2017). Using RNAi to knock down expression of this regulatory gene, it was also shown to not only play a role in nutrition dependent horn development (Kijimoto, Moczek, & Andrews, 2012), but also to modulate aggressive behavior in different ways in males and females. These results suggest that a single switch is involved in morphological and behavioral aspects of the alternative reproductive tactics in the dung beetle (Beckers, Kijimoto, & Moczek, 2017).
Ongoing work in the pea aphid (Acyrthosiphon pisum), another extremely complex integrated phenotype, further demonstrates the value of considering all aspects of reproductive plasticity while maintaining an ecologically-oriented approach. In this species, there is both a set of alternative male strategies based on a genetic polymorphism (Braendle, Friebe, Caillaud, & Stern, 2005) and female reproductive plasticity in the form of alternative tactics that, while influenced by genotype, are largely triggered by the environment (Vellichirammal, Madayiputhiya, & Brisson, 2016). Both the male and female alternatives include a wingless and a winged morph, the latter of which is triggered in females by population density, facilitates dispersal, and has lower reproductive output (Hille Ris Lambers, 1966, reviewed in Brisson, 2010). Even the option to produce males and sexually reproductive females represents an additional reproductive trade-off for the female’s allocation of resources, which allows autumnal sexual reproduction in addition to summertime asexual reproduction.
While transcriptomic data in this system has largely been addressed through the lens of morphology and metabolism, this system is primed for analysis of behavior and understanding how genetic and environmental factors interact (Brisson, Davis, & Stern, 2007). The diversity of plastic reproductive phenotypes in insects can be capitalized on by using a comparative approach such as was done with transcriptomic data from the fire ant, Solenopsis invicta. When the queen is experimentally removed, virgin winged females compete for dominance to become queen, rather than engaging in their normal mating (Wurm, Wang, & Keller, 2010) and the gene expression changes associated with this transition show significant overlap with those associated with queen status in honeybees (in the brain) (Grozinger, Fan, Hoover, & Winston, 2007) as well as with genes specifically expressed due to mating experience in honeybees (in the ovaries) (Kocher, Richard, Tarpy, & Grozinger, 2008) and mosquitos (whole body) (Rogers et al., 2008), but not flies (McGraw, Gibson, Clark, & Wolfner, 2004).
These studies exemplify the need to study the mechanisms underlying the different aspects of reproduction in parallel (behavior but also physiology and morphology), based on the assumption that pleiotropic effects may be necessary to produce complex integrated phenotypes. While much of the focus of these and other transcriptomic studies in insects (e.g., bulb mites Stuglik, Babik, Prokop, & Radwan, 2014) relates to morphological development, it is important to remember that these phenotypes are systematically and dramatically different in terms of behavior, physiology and reproductive tactic. Studying all aspects of reproductive plasticity linked together in an integrated phenotype will bring a better understanding of its evolution.
Sex-Role Reversal and Sex Reversal
The instances of reproductive plasticity described thus far include shifts in behavior, reallocation of resources, and morphological changes, even including gonadal atrophy to some degree, but sexual expression (the production of sperm versus eggs) remains static in most organisms. Beyond the within-sex plasticity for (primarily) male ARTs, there are instances of reversal of sex-biased behavior. When individuals that produce sperm invest more in offspring than individuals that produce eggs, a species is said to be sex-role reversed and sexual selection acts more strongly in females than males (Eens & Pinxten, 2000). In these species, females tend to compete and males tend to choose.
The existence of fully sex-role reversed species (e.g., signathids) offers unique opportunities to enhance our understanding of the mechanisms mediating behavioral sex differences and test assumptions from one sex applied to the other (Eens & Pinxten, 2000). As such studies have just begun at the genomic level (e.g., pipefish: Beal, Martin, & Hale, 2018), other systems that exhibit sex-role plasticity in response to the environment can be particularly informative. Potentially promising systems include the facultative sex-role reversal of tettigoniid bushcrickets, in which males invest by producing nutritious spermatophores that allow for conventional sex-roles on high-quality diets, but promote sex-role reversal and male choice on low-quality diets (Ritchie, Sunter, & Hockham, 1998). Similarly, in the two-spotted goby (Gobiusculus flavescens), the environment produces sex-role plasticity since as the operational sex ratio becomes female biased over time, the early-season male-male competition gives way to late-season female-female competition (Forsgren, Amundsen, Borg, & Bjelvenmark, 2004).
On an evolutionary timescale, two species of the cichlid genus Julidochromis have evolved different sex-biased behavior patterns, but plasticity still plays a role: while J. transcriptus predominantly follows the ancestral pattern of male dominance, male-biased sexual size dimorphism and territoriality, a minority of pairs in the wild express a reversal of this sex-biased pattern (Awata & Kohda, 2004). For J. marlieri, the predominant sex-biased pattern is naturally reversed, such that females show these male-typical behaviors and morphology (Barlow & Lee, 2005; Wood, Zero, Jones, & Renn, 2014). Comparing brain transcriptomes between species suggests a pattern associated with behavioral phenotype and independent of gonadal phenotype. In general, these data suggest that while there has been substantial divergence in gene expression patterns between these two species, there remains a core set of genes related to aggression (Schumer, Krishnakant, & Renn, 2011). Comparing the neural transcriptome of plastically aggressive J. transcriptus females with that of stably aggressive J. marlieri females suggests that a subset of this core set of genes related to aggression is also involved in a short-term plastic switch to aggression (M. Schumer & S. Renn, unpublished data). Further examination of species in which sex-biased behaviors are plastically reversed or evolutionarily labile will help separate the mechanisms related to behavior versus gonadal sex.
In some teleost fishes, the only vertebrate lineage to exhibit sequential hermaphroditism, plasticity of reproductive phenotype is so extreme that individuals naturally reverse sexual expression (the production of sperm versus eggs) and undergo actual sex change. Sex change is typically triggered by changes in social structure or attainment of a critical age or size (Warner, 1984). In these species, sexual phenotype is not final but rather must be maintained by suppression of one molecular network and activation of another. The opposing sexual network creates the potential for flexibility that is retained into adulthood. Sequential hermaphrodites begin their reproductive stage as one sex, changing sometime later to the other. This process includes protandry (male-to-female), protogyny (female-to-male), and serial (bidirectional) coordinated changes in behavior, anatomy, endocrinology, physiology and molecular processes (reviewed in Todd, Liu, Muncaster, & Gemmell, 2016; Liu et al., 2017).
For example, a comparative study examined brain transcriptomes of two sparid fish species that exhibit protogynous hermaphroditism (Pagellus erythrinus and Pagrus pagrus) by sampling endpoint animals collected from the wild. While only zona pellucida genes were up-regulated in females of both species, males (the final sex) of both species showed increased expression in genes related to synaptic function, neurotransmitter receptor trafficking, MAP-kinase regulation and ephrin signaling, several of which have previously reported in mammalian sex determination or neuronal activation in a reproductive context. Furthermore, the males showed increased expression of genes related to immediate early gene signaling, a marker of neuronal activity (Tsakogiannis et al., 2018). Overall, these comparative studies showed that a fish brain is not entirely irreversibly sexualized and that female-related transcription signatures can give way to male specific patterns, epitomizing the plasticity of the fish brain.
Transitions within an individual’s lifetime give us the opportunity to sample the final “endpoint” phenotype, but also to take advantage of a time series approach by sampling between the endpoints. The advantage of studying the transition through a time series is that a dynamic view of gene expression allows us to detect genes that are only transiently expressed, as is often found in developmental biology transcriptomics experiments (Graveley et al., 2011; Trapnell et al., 2010; see “In Which Systems Should We Study Proximal Mechanisms?”). Studying the sequence of events during the transition from male to female in a species with a temporal asynchrony between the behavioral and gonadal shifts allows us to detect mechanisms that are the causes versus those that are the consequences of sex change (Aubin-Horth & Renn, 2009; Rittschof & Hughes, 2018).
In a model protogynous species, the bluehead wrasse, reproductive plasticity includes not only the possibility to change sex from female to male but also the potential to develop directly as a sexual male (triggered by population density) with an alternative sneaking phenotype known as an initial-phase that can later transition to the brightly colored territorial terminal-phase male (i.e., diandric protogyny) (Warner & Swearer, 1991). For females, when the terminal phase male is removed, behavioral sex change can begin within minutes to hours independent of the gonads while functional gonadal sex change takes up to a week (Godwin, Crews, & Warner, 1996). Similar to other studies of alternate male morphs in fish (see ARTs) forebrain gene expression differences among phenotypes are more closely associated with behavioral differences than with gonadal phenotype, such that the greatest number of differentially expressed genes were found between initial and terminal phase males, while the neural gene expression profile of initial phase males was more similar to females (Todd et al., 2018) despite dramatic differences in gonadal gene expression (Liu et al., 2015).
While the role changes from initial to terminal phase male is less common than sex change, this system offers the potential to compare terminal phase males derived from different reproductive phenotype histories. Similarly, in a model protandrous species, the Red Sea anemonefish (Amphiprion bicinctus), the behavioral changes seen when a male switches to a female role occur before the gonads have changed to fully-functional female. The time series comparing the neural transcriptome of males compared to transitional male (behaviorally female), transitional female, immature female and mature females shows that while males show a response to removal of the dominant female that leads to behavioral sex change after two weeks, gonads show a transcriptional response only after three to four weeks. In the brain, there is a clear gene expression pattern that separates individuals in transition from male to female compared to “stable” male and female phenotypes, with many genes being down-regulated during the transition (Casas et al., 2016).
Bidirectional hermaphroditism is less common and only known to occur in a handful of protogynous species that retain the ability to revert to female after the initial transition to male (Manabe et al., 2013). Few studies have examined the hormonal or gene expression changes associated with bidirectional sex change, though one study identifies sf1 gene expression correlated with expression of the female phenotype during a shift in either direction (Kobayashi et al., 2005). Further genome-level studies with these species should be informative with regard to the modularity of gene expression, the synchronicity (or lack) of transcriptomes form different tissues with the organismic phenotype at the behavioral and physiological levels during transition, and the degree to which temporal sequence of these modules is directly reversed or transposed for each direction.
Studying Model Systems
Interestingly, while ethologists herald Krogh’s principle (Krogh, 1929), advocating for the importance of studying taxonomically diverse organisms, a few of our traditional model organisms also offer an as yet untapped insight into the mechanisms behind alternative reproductive phenotypes. For example, Daphnia, which have long been studied as a model of phenotypic plasticity with regard to morphology, also can reproduce sexually or asexually, though no mechanistic studies have addressed the alternative behaviors associated with this dramatic switch. Furthermore, males are produced plastically in response to environmental signals, presenting another form of reproductive plasticity in this species to be studied mechanistically (Molinier et al., 2018). Similarly, the model nematode C. elegans can either outcross or self-fertilize, but transcriptomic studies in these organisms have focused on sex-biased expression rather than plasticity and variation associated with these alternate phenotypes within a sex (e.g., Fagan & Portman, 2014). These systems could provide valuable models, though to date less has been done related to behavior of these organisms.
ARTs in Birds
Aside from the few mechanistic studies of cooperative breeding and the initial studies for facultative brood parasitism, the majority of research regarding the diversity of reproductive phenotypes among birds has centered on instances of alternative genetic strategies, rather than phenotypic plasticity. Similar to the recent identification of genomic inversions as the basis for the genomic architecture of reproductive strategies in the ruffs (see introduction), a “supergene” capturing genes that influence HPG function and androgen plasma levels is known to be the cause of the two morphs (white and tan stripe) in the white-crowned sparrow (reviewed in Maney, 2008). Interestingly, and similarly to the Gouldian Finch, in which head colour polymorphism is determined by two genes also impacting hormonal profiles (Brazill-Boast, Griffith, & Pryke, 2013), the sparrow genetic polymorphisms lead to alternative strategies in both males and females (Kokko et al., 2014; Pryke & Griffith, 2007), however, in the sparrows reproductive success is greatest for individuals that pair with the opposite morph. Future study will be necessary to determine the extent to which these genetic polymorphisms, often chromosomal inversions, affect the same genes that are dynamically regulated in the plastic phenotypes of other species. Furthermore, it will be important to understand the constraints acting on the evolution of reproductive plasticity to determine if the absence of plastic ARTs in birds in the literature stems from a research bias or reflects differences from other vertebrates such as fish, and, if the latter is true, what factors are driving this divergent evolutionary pattern.
Historically, studies of intrasexual selection and competition have mainly focused on males. This bias in research is owed in part to the more exaggerated traits that are more easily studied. However, females show territoriality, aggression (birds: Pryke, 2007), and dominance relationships, and compete for access to resources that can translate to reproductive benefits (primates: Pusey, Williams, & Goodall, 1997; meerkats: Russell, Carlson, McIlrath, Jordan, & Clutton-Brock, 2004).These set the stage for intrasexual selection and competition that facilitate the development of plastic reproductive behavior, such as reproductive suppression, competition for quality mates, and even infanticide (reviewed in Stockley & Bro-Jørgensen, 2011). It is thus imperative to fill the absence of female-centered studies.
A rare study of a female ART is found in the striped mouse; in this system, females breed communally or solitarily, employing different reproductive tactics depending on the individual’s condition (Hill, Pillay, & Schradin, 2015a). Given current data describing the different hormonal profiles associated with these phenotypes, this system is ready for a genomic approach to identify transcriptomic changes associated with female reproductive plasticity (Hill, Pillay, & Schradin, 2015b). Male striped mice also exhibit alternative tactics with three phenotypes; paternal group-living breeders, alloparental philopatric group-living males, and roaming non-paternal solitary males. While not yet addressed for females, prolactin levels vary according to male reproductive phenotype with that of breeders being significantly higher than that of roamers and alloparental philopatric males (Schradin, 2008), a pattern that differs from that seen in cooperatively breeding birds in which the alloparental individuals also show increased prolactin (Buntin, 1996).
These systems highlight the need to study male and female reproductive plasticity concurrently, as their physiology and behavior are interrelated and the phenotypes of the partners will affect the fitness and possibly the phenotype of the opposite sex (Brockmann, 2002).
Finally, whether different reproductive phenotypes represent distinct genetic strategies or are alternate tactics resulting from a single strategy, any underlying genetic architecture that is not strictly sex-linked has the potential to influence both sexes, though possibly with unequal penetrance. Although alternate reproductive strategies and tactics are largely studied and discussed in terms of the male mophs, several of the classic textbook examples include alternate phenotypes in females too (e.g., Gouldian finch: Pryke & Griffith, 2007; side-blotched lizard: Alonzo & Sinervo, 2001; common guillemot Kristensen, Erikstad, Reiertsen, & Moum, 2014).
Molecular Encoding of the Environmental Signal
The one area in which female reproductive phenotypes have begun to be addressed at a mechanistic level is that of mate choice, which interestingly is as female biased as the study of ARTs is male biased. While these studies have so far primarily focused on identifying the brain regions involved in female choice, it should be noted that males make choices as well, both with regard to mates (either courted or coerced) and with regard to which males to cuckold when sneaking copulations. In both sexes, sensory reception and processing are plastic, either tracking seasonal changes or linked to changes in the social environment and reproductive phase of individuals (reviewed in Lynch, 2017).
Auditory thresholds differ according to male dominance status and female reproductive state in the cichlid fish A. burtoni (Maruska, Ung, & Fernald, 2012) and female condition in the round goby, N. melanostomus (Zeyl et al., 2013), while electrosensory tuning in elasmobranch fishes (Sisneros & Tricas, 2002), auditory resolution in sparrows (Caras, Sen, Rubel, & Brenowitz, 2015) and olfactory sensitivity responsible for pheromone detection in carp (Hamdani, Lastein, Gregersen, & Doving, 2008) vary with season. While a transcriptomic approach has been applied to the saccular auditory system of the alternate male morphs in the benthic vocal midshipman (Faber-Hammond et al., 2015), and the initial processing cells of the startle response in A. burtoni (Whitaker et al., 2011) the majority of studies that address plasticity in the periphery have examined only hormonal sensitivities (sparrow: Caras, Brenowitz, & Rubel, 2010) or candidate genes (e.g., opsins in damselfish (Stieb, Carleton, Cortesi, Marshall, & Salzburger, 2016). The flexible response of males to different social cues in a reproductive context has also been addressed by comparing the effects on olfactory bulb and olfactory pallium gene expression in dominant, reproductive male fish of exposure to odors from females at different time points in their reproductive cycle, and from males of divergent dominance status (tilapia: Simoes et al., 2015).
Comparing the response to different stimuli allows us to separate the general response to a particular sex from the inherent valence of the particular stimulus. For example, males showed unexpected similarities in response at the transcription level when exposed to seemingly very different cues, such as the odors of subordinate males and pre-ovulatory females, or of dominant males and post-ovulatory females (Simoes et al., 2015). An important role for molecular changes in the periphery has long been appreciated in the production of dominance hierarchies (Edwards et al., 2002) and could similarly be a profitable area of research for studying plasticity of not only mate choice but other plastic reproductive phenotypes as well.
Fitness and Reproductive Plasticity
A central assumption of evolutionary theory regarding the evolution of plastic phenotypes in general is that expressing a given phenotype in response to a certain environmental signal (internal or external) maximizes fitness in the future environment that this signal predicts, versus expressing an alternative phenotype or not exhibiting any plasticity (West-Eberhard, 2003). This has also been argued for reproductive plasticity, for example in the case of ARTs (Hazel, Smock, & Johnson, 1990; Hutchings & Myers, 1994; Roff, 1996). However, this relationship between expressing a certain plastic reproductive phenotype and fitness is hard to test, mainly because one needs phenotypic variation within a given tactic to link it to fitness variation, which is not always present in natural populations. Using experimental manipulations to create diversity allows one to test this relationship, but results do not always support this basic assumption of the evolutionary model (Michalczyk, Dudziak, Radwan, & Tomkins, 2018). Knowing more about the mechanisms underlying the development of certain plastic phenotypes will provide molecular and hormonal targets to experimentally manipulate individuals, with the goal of creating high and low condition individuals of each phenotype, an approach often termed “phenotypic engineering” (Ketterson, Nolan, Cawthorn, Parker, & Ziegenfus, 1996).
Plasticity as a Leader in Evolution
An important question to answer is whether the same or different mechanisms are used for genetically-fixed versus plastic reproductive strategies, which is important to know if we aim to determine whether plastic traits are the first step leading to genetically determined phenotypes (Ghalambor et al., 2015; West-Eberhard, 2003). Understanding the mechanisms underlying genetically fixed reproductive strategies and plastic reproductive tactics demands that we compare plastic systems to genetically based systems, in order to determine if the same transcriptional pathways are at play (Fraser et al., 2014; Renn & Schumer, 2013). The study of ARTs in fish provides a first glimpse at the possibilities that comparing plastic tactics (e.g., Atlantic salmon) and genetically fixed strategies (mollies) will bring, for example to understand how neural plasticity seems crucial in both cases.
A note of caution: while comparative studies and meta-analyses between species (Renn et al., 2016, 2017; Rittschof et al., 2014) allow one to identify evolved differences in regulatory mechanism associated with behavioral variation, such studies often involve comparisons between groups based on samples that vary in tissue composition. On the one hand, this can introduce variation in relative RNA abundance resulting in a pattern that can be erroneously detected as differential expression, as demonstrated by mathematical models (Montgomery & Mank, 2016). On the other hand, an absence of concordance in gene expression for a given gene may be found, while a broader look at biochemical and signal transduction pathways and whole gene networks may actually show large similarities (Rittschof & Robinson, 2016; see “In Which Systems Should We Study Proximal Mechanisms?”). Furthermore, eventually, all the biological levels should be studied rather than focusing solely on transcription, as they are all crucial and interact with each other. Ideally, we would combine information from different biological levels of organization (neurological, biochemical, transcriptional, hormonal, immunological, and so on; Zera & Brisson, 2014) to obtain a complete functional picture of the genotype-phenotype map.
Convergent Evolution at the Behavioral and Molecular Level
Species that show a similar plastic reproductive phenotype, which we would call convergent phenotypic evolution, may actually not express these similar traits by activating and repressing the same molecular pathways. Whether there is convergent evolution also at the molecular level is still largely unknown, with most work done thus far focused on a few candidate genes (see O’Connor et al., 2015). In order to move beyond a candidate gene approach and produce cohesive theories regarding molecular evolution of transcriptomic mechanisms on a genomic scale, it is helpful to build a research community that will produce several studies that include ecological, evolutionary and mechanistic information, giving rise to a rich body of literature and multiple related examples that can be compared by including phylogenetic relationships. Recent meta-science data has indeed shown that collaborations and multidisciplinary endeavours enhance scientific impact (Fortunato et al., 2018). The work being done to examine eusociality in different insects has begun to enjoy such momentum in producing cohesive theories from the initially conflicting data. Furthermore, work on hymenoptera shows that combining transcriptomics with genomics data allows one to detect divergence in gene sequences and also how novel genes are implicated in the evolution of a phenotype such as high eusociality. Similarly, the numerous studies on fish ARTs have also provided a picture of the type of molecular pathways that are modified again and again in males exhibiting alternative ways to access reproduction (neural plasticity, memory), such as sneakers. The emerging trend is that it is not an either/or evolutionary situation, as important pathways are shared, but novel genes also play a role (see Rittschof & Robinson, 2016, for a discussion of all the alternative hypotheses associated with the behavioral genetic toolkit).
What Are “Proximal Mechanisms”?
Plastic reproductive phenotypes are integrated phenotypes that arise from a specific combination of morphology, physiology, and behavior. All of these coordinated changes are expected to be implicated in increasing fitness. To understand how these integrated phenotypes come to be, we must study what changes within the lifetime of an individual to produce these (potentially) adaptive phenotypes, as these different phenotypes do not result from genetic polymorphisms. Proximate mechanisms are defined as “the causal factors of animal behavior found at different levels of biological organisation” and are studied in the context of the physiology of behavior (Tinbergen, 1963). Studying the pathways that lie between the genome and the observed organismic phenotype involves considering several interconnected mechanisms within the biological level of molecular and cellular organization: gene transcription levels, alternative splicing, protein levels, post translational modifications (which affect among other things the activity of proteins, their life span and their location), as well as labile factors that control the synthesis of these proteins, such as epigenetic marking (histone modifications, DNA methylation, etc.), and small RNAs that affect which mRNA is translated to a protein (reviewed in Jaenisch & Bird, 2003).
One very fruitful approach in the study of plastic phenotypes in general has been the study of hormones, as they often control the development and expression of several traits (Zera & Brisson, 2014). Indeed, one of the major roles of hormones is the control of downstream gene expression, which in turn affects physiology and development. If we want to understand what is needed to build a functional reproductive individual, which involves not only the reproductive axis but also behavior (courting, aggression/dominance, defense, care, change in energy acquisition/feeding), we need to also get an overview of interacting physiological functions without necessarily having an a priori knowledge of the biological functions involved. One way to obtain this overview is by using large-scale “omics” approaches, which aim to measure all molecules present in a given sample, such as all the mRNA or all the proteins present in a cell or tissue. All the biological levels of organization found between the genome and the organism are crucial and interact with each other, namely molecules, cells, tissues, physiological systems (including hormones, immune system, metabolism), physiological regulatory networks, and the whole organism (Martin, Ghalambor, & Woods, 2015). However, at this stage in tool development, the most used and accessible large-scale approach is transcriptomics, the study of all the mRNAs in a sample (the transcriptome: Velculescu et al., 1997). The original tools to study the transcriptome were microarrays, subtractive hybridization, differential display, and the like, but high-throughput sequencing such as RNA-seq is now more commonly used. Independently of the method used, transcriptomics allow us to study the plastic response for a large range of timescales, from minutes to years after exposure (reviewed in Rittschof & Hughes, 2018).
In Which Systems Should We Study Proximal Mechanisms?
The comparative approach is defined as studying the same trait in different species/taxons. By taking a comparative approach when enough species have been studied, we gain information on the evolution of the physiological regulatory pathways (Martin et al., 2015). We attain this by comparing which genes and functions are plastically regulated in independently evolved plastic reproductive traits, in order to determine if the same pathways are “re-used” over and over, if the downstream signaling of these same pathways effectively leads to the same organismic phenotypes, or if novel genes are key to these independent phenotypes (Rittschof & Robinson, 2016). Furthermore, by taking a comparative approach, we can uncover whether the genes that are plastically regulated are the same genes that are implicated in divergent reproductive phenotypes that result from evolutionary genetic divergence. Indeed, it has been suggested that plastic reproductive phenotypes and evolved genetically-determined reproductive phenotypes rely on separate underlying mechanisms to produce the divergent phenotypes (Ghalambor et al., 2015). However, other studies suggest evolutionary relationships between these different timescales (Fraser et al., 2014; Mäkinen, Papakostas, Vollestad, Leder, & Primmer, 2016; Whitehead, Pilcher, Champlin, & Nacci, 2012) through the process of genetic accommodation, where a phenotype once resulting from developmental plasticity becomes constitutively expressed by selection over evolutionary time (Renn & Schumer, 2013; West-Eberhard, 2003). This debate regarding the shared or independent nature of molecular and physiological networks governing divergent reproductive phenotypes of plastic and genetic origin can be addressed by mechanistic studies involving gene expression. While this review focuses on the gene expression patterns associated with phenotypic plasticity, comparisons to instances of evolutionary divergence in reproductive phenotypes are thus also important.
When Should We Study Proximal Mechanisms?
Studying the expression of all genes in distinct phenotypes allows us to draw a picture of these phenotypes: are a few or many genes differentially expressed? where and what are their functions? (mate choice: Cummings et al., 2008; reproductive investment: Renn et al., 2008; ARTs: Aubin-Horth, Landry, Letcher, & Hofmann, 2005a). What we obtain with these endpoint studies is an association between phenotypes at different levels of organization: molecular and organismic. These associations provide an enormous amount of information to understand the functional aspects of development of plastic phenotypes, which are a prerequisite not only to testing hypotheses about its evolution but actually creating the framework within which we can generate hypotheses (Zera & Brisson, 2014). However, these “endpoints” of development are the result of a process, and it is possible that some of the genes that have lead to this phenotype may have been transiently expressed during development but are not detectable or not differentially expressed at the endpoint (Aubin-Horth & Renn, 2009; Rittschof & Hughes, 2018). To go beyond the correlation and get at causation, and be able to separate cause from consequence, we thus must study different points in time following exposure to the environmental signal resulting in the plastic phenotype. Importantly, studying a plastic phenotype that can be induced in controlled settings by manipulating the environmental conditions allows us to study the various intermediate transcriptomic states leading to the final reproductive phenotype. As an example, a follow-up study to a transcriptomic analysis of endpoints of reproductive suppression in fish (Renn et al., 2008) using a candidate gene expression approach, showed that the intermediate phenotype between a reproductively suppressed subordinate male and a reproductively active dominant male, called an “ascending male,” had the largest changes in gene expression for an candidate gene and its receptor (Huffman et al., 2015). Such a time series approach will ultimately bring us closer to the initial signaling cascade that triggers the plastic developmental program, which is still poorly known (see “Future Directions”).
The work highlighted here supports several points that are worth summarizing (Figure 1). Because sexual reproduction, a pivotal event of an individual’s life, is subject to selective forces from other individuals of the same sex and the opposite sex, as well as environmental conditions, evolution has resulted in a diversity of reproductive phenotypes, many of which are adjusted through plastic processes as means to increase fitness. Here we have highlighted how mechanistic studies, particularly genomic scale gene expression studies, can be applied to the study of these plastic reproductive tactics that range from subtly different to very divergent and change reversibly or irreversibly on different timescales. Overall, this survey of various types of reproductive plasticity shows that they inform each other by highlighting genes, pathways, and biological functions that are repeatedly co-opted to create these different phenotypes.
Mate choice, while not always appreciated as plastic and as a reproductive behavior, can be sensitive to distinct social/reproductive contexts or past experience which can alter gene expression, often related to nonapeptides, hormone synthesis, and synaptic plasticity. By localizing and comparing gene expression responses to preferred and non-preferred stimuli, we may be able to address the inherent valence of the stimulus for different individuals or in different contexts. Parental care has long been studied as a trade-off considering the investment to current offspring versus future offspring, and the mechanisms of maternal care are well studied in mammals (Numan, 2012). However, for the majority of species in which allocation of care is decided by one or both parents, the mechanisms underlying the decision have yet to be investigated. Available data shows that in some cases, seemingly similar parental behaviors do not correlate with equivalent gene expression profiles, yet some between-species differences mirror those seen within a species. Also, parental brains of both sexes show gene expression changes that overlap but that also show their particular signature. Reproductive suppression, which can be highly reversible (flexible dominance hierarchies) or absolutely fixed in early development (castes) has been well studied in many species, often revealing what appear to be species-specific patterns of hormonal or gene expression regulation, suggesting that many aspects of the underlying biology can evolve to produce these apparently convergent behaviors. Comparisons between species, with attention to phylogenetic relationships as well as the ecology and natural history of the organism, will be necessary in order to develop overarching theories and understand not only how these phenotypes are orchestrated but also how they evolve. Support both for shared “genetic toolkits” across species and for specific genomic signatures are found. There are numerous genomic-scale studies on the ARTs found in teleosts, while most of the research conducted on avian reproductive phenotype diversity has focused on alternative strategies and their genomic polymorphisms. This bias is likely due in part to the relative ease of recapitulating many of the teleost social systems in a controlled experimental setting, facilitating the extraction of RNA for transcriptomics, but may also be impacted by the rarity and general aesthetic appeal of the birds making them more amenable to DNA sampling only. Regardless of the reasons for this bias, there exist many avian systems in which we could test some of the patterns repeatedly identified in fish. For the most part, we see that the plastic reproductive tactic is more strongly correlated with differential gene expression than sexual dimorphism is. In some cases, the genes that differentiate the sexes are also involved in the differentiation of phenotypes within a sex, but species-specific patterns, and even species-specific genes may underlie some aspects of the behavioral phenotypes. Here, the dramatically different phenotypes seen in many ARTs make evident the need to study all aspects of reproductive plasticity that is linked in an integrated phenotype, and that studying tissues other than the brain may provide insight into the mechanism that respond to the environment and initiate the developmental path to one phenotype or the other. The most dramatic of the plastic reproductive phenotypes is that of sex change, a system in which a time series is necessary to capture the dynamic view of gene expression in order to fully understand the process. While a detailed time series may begin to elucidate the functional relationship of different gene modules, follow-up studies that experimentally manipulate gene expression and hormones paired with further transcriptome analyses will be necessary to identify causal aspects of the observed gene expression patterns.
Members of the Aubin-Horth and the Renn lab read earlier drafts to provide comment: Frankie Williams, Gabe Preising, Rose Driscoll, Marie-Pier Brochu, Verônica Alves, Caroline Côté, Maël Balanec. We thank an anonymous reviewer for a thoughtful review that guided us to greatly improve this manuscript.
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