Sensitive periods during the development and expression of vertebrate sexual signals: A systematic review

Abstract Many sexually selected traits exhibit phenotypic plasticity. Despite a growing appreciation for the ecological context in which sexual selection occurs, and for the role of plasticity in shaping traits associated with local adaptation and divergence, there is an important gap in knowledge about the onset and duration of plasticity in sexual trait expression. Integrating this temporal dimension of plasticity into models of sexual selection informs our understanding of the information conveyed by sexual traits and our predictions related to trait evolution, and is critical in this time of unprecedented and rapid environmental change. We conducted a systematic review of 869 studies to ask how trait modalities (e.g., visual and chemical) relate to the onset and duration of plasticity in vertebrate sexual signals. We show that this literature is dominated by studies of coloration in birds and fish, and most studies take place during the breeding season. Where possible, we integrate results across studies to link physiology of specific trait modalities with the life stage (e.g., juvenile, breeding, or nonbreeding) during which plasticity occurs in well‐studied traits. Limitations of our review included a lack of replication in our dataset, which precluded formal analysis. We argue that the timing of trait plasticity, in addition to environmental context, is critical for determining whether and how various communication signals are associated with ecological context, because plasticity may be ongoing or occur at only one point in an individual's lifetime, and determining a fixed trajectory of trait expression. We advocate for careful consideration of the onset and duration of plasticity when analyzing how environmental variation affects sexual trait expression and associated evolutionary outcomes.


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McDERMOTT anD SaFRan Cornwallis & Uller, 2010) and that the evolution of multiple signals may be selected for because each trait conveys unique information about the signaling animal ("multiple message hypothesis" ;Møller & Pomiankowski, 1993). Indeed, decades of research has identified (1) specific examples of plasticity in sexual traits, and (2) the types of environmental factors that influence expression of sexual traits. For example, parasite load influences male color of house finches (Haemorhous mexicanus) (Hill & Farmer, 2005;Thompson et al., 1997), and diet quality influences attractive chemosignals of Iberian mountain lizards Iberolacerta monticola (Martín & López, 2006. Research on sexually selected traits has shown that the degree of trait exaggeration is associated with environmental context (Martín & López, 2015;Scheuber et al., 2003a;Thompson et al., 1997).
However, we still lack a clear understanding about the timing of trait sensitivity to the environment throughout an individual's life (e.g., "static" vs. "dynamic" signals; sensu Hebets & Papaj, 2005). Research in human learning and mammal behavior has, for decades, recognized the existence of "sensitive periods" in development during which environmental influences (esp. social interactions and neurotoxins) have a profound effect on developmental trajectories (Illingworth & Lister, 1964;Rice & Barone, 2000). Many neural traits show patterns of developmental plasticity (Bateson et al., 2004;Stamps, 2016;West-Eberhard, 2005), which we define here as traits that are most sensitive to environmental variation in early life. Studies of insect metamorphoses and migration show that plasticity can be induced by seasonal changes in the environment, that is, seasonal plasticity (Nylin, 1992;Nylin et al., 1989). Behavioral ecologists recognize how moment-to-moment changes in the environment alter an animal's behavior, that is, continuous or contextual plasticity (Stamps, 2016).
These types of plasticity differ in onset and duration of a sensitive period in trait expression (Table 2).
Understanding the physiological mechanisms underlying sensitive periods more generally, and the implications for evolution, is a topic of intense recent interest and an explosion of research (Boyce et al., 2020;Reh et al., 2020;Sanz et al., 2020). While theories of multiple signal evolution have acknowledged the roles of both timing of sensitive periods and type of environmental variable (e.g., parasites vs. nutrition) as contributing to the information conveyed by signal traits (Candolin, 2003;Møller & Pomiankowski, 1993), empirical work on sexually selected traits is usually designed to detect types of influential environmental variables (Cornuau et al., 2014;Hill et al., 2009;Rahman et al., 2013) rather than timing (but see Scheuber et al., 2003aScheuber et al., , 2003b for excellent counterexamples).
Researchers examining the physiological basis of sexual signals likely choose to study their animals during a stage they believe to be sensitive to a particular environmental variable based on their prior knowledge of the system, but this is rarely if ever made explicit.
In sexual selection research, environment-trait linkages are frequently described as condition dependence (Andersson, 1986;Hill, 2011;Rowe & Houle, 1996;Warren et al., 2013). Although there is much debate about how to define and measure condition (Wilson & Nussey, 2010), condition dependence is increasingly conceptualized as a special case of phenotypic plasticity in which trait expression is exaggerated when an individual experiences favorable environments (Cornwallis & Uller, 2010;Fox et al., 2019;Price, 2006), for example, bright coloration in an individual with access to a high-quality diet or no parasitic infections (Hill & Farmer, 2005;Ruell et al., 2013).
Accordingly, to adopt consistently defined terminology, we refer to the environmental influences on trait development and expression as the extent to which a trait exhibits plasticity.
In this review, we seek to integrate an explicit consideration of sensitive periods in sexual trait expression with decades of research focused on the evolution of sexually selected traits. Considering  Zahavi (1975). b Hamilton and Zuk (1982).

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McDERMOTT anD SaFRan the temporal dimension of plasticity in sexually selected traits may help to integrate results that at first seem contradictory but instead point to variation in the sensitivity to the environment during trait development or expression. For example, food quantity seems to affect song frequency in Taeniopygia guttata during the juvenile stage (Woodgate et al., 2014) but not during the adult stage (Ritschard & Brumm, 2012 (Buchanan, 2011). Scenarios where there is a delay between the environmentally sensitive period and changes in trait expression have been highlighted as a mechanism by which plasticity in sexual traits may erode signal reliability (Ingleby et al., 2010), but they may also be informative, as when traits are correlated with the quality of parental care received by an individual and thus likely to be provided by that individual (Hoelzer, 1989;Wolf et al., 1997).  (Ingleby et al., 2010). Seasonally grown traits may also be evolutionarily constrained and not ideal signals of mate quality. Bird feathers, for example, must be molted to maintain flight performance, but, once regrown, are mostly dead tissues and pigment deposition ceases.
Continuous plasticity. If a trait is continuously sensitive (plastic) throughout its lifetime, that trait may provide a reliable real-time readout of an individual's ability to cope in a particular environment. For example, chemical signals can change with relatively short-term changes in diet or stress (e.g., Martín & López, 2006). There is little delay between changes in the environment and changes in trait expression. Thus, potential mates are able to assess the recent or real-time health of the signaling animal. This may be particularly relevant when direct benefits or territory quality are critical for ensuring the survival or reproductive success of the mate or offspring.

BOX 1 (Continued)
dependence" as well as "plasticity" in our searches as this is the most widely used terminology across years and taxonomic groups to study trait plasticity in the context of sexual selection.
We systematically screened all titles and abstracts and, if necessary, methods and results to exclude papers that: were on invertebrates, only considered traits other than sexually selected pre-mating traits (e.g., sperm or a naturally selected trait), did not contain data at the level of the individual, were not empirical (e.g., reviews or theoretical studies), or did not manipulate or measure an environmental variable ( Figure 1). We chose to focus on vertebrate research here to fill a gap in the literature about sexual selection and plasticity. To our knowledge, no such review exists for vertebrates; however, similar topics have been touched on in reviews focused on invertebrates (Hunt & Hosken, 2014;Ingleby et al., 2010). In addition, we hoped to make some generalizations about physiological mechanisms behind trait expression at particular life stages, which would not be possible when reviewing vertebrates and invertebrates together. We further wished to focus on the information potential mates can obtain from signal traits, and therefore, we did not include papers on post-copulatory traits or those used primarily in male-male aggression, although these are certainly interesting and exciting subjects of study (for a nice review of behavioral plasticity in pre-and post-copulatory traits, see Bretman et al., 2011). We focused on papers that had manipulated an environmental variable of interest (hereafter "experimental studies") or those that used a repeated-measure design to track individual change over time in response to environmental change (hereafter "longitudinal studies").
Observational studies without repeated measures (i.e., individuals are measured at only a single point in time) cannot detect plasticity, since any correlations between trait and environment could be due to genetic differences, plasticity, or both.
We thoroughly read and scored all selected papers with particular attention to life stage, study design (experimental, longitudinal, or both), types of environmental variables, types of traits, and the quality of evidence that the trait of interest is sexually selected.
For a detailed list of scoring criteria and notes, see Table S2. We ensured consistency by having both observers [MTM and RJS] score the same set of five papers and refined our definitions in light of any discrepancies. We repeated this process for four sets of five papers until we had complete agreement in scoring among observers.
Afterward, papers were scored independently. Any papers where we felt uncertain about categorization were scored together.
To answer our driving questions about the state of the literature in the context of the timing of sexual trait plasticity, we summarized the distribution of papers among years, taxa, traits, environmental variables, experimental designs, and life stages. We also summarized the number of traits or environmental variables studied by these papers. To gain a deeper understanding of the findings of this body of literature, we identified traits in our database that (1) were studied across multiple life stages, (2) had good evidence for being sexually selected, that is, were correlated with mating or reproductive success, and (3) were measured in a relatively consistent way such that a synthesis across studies was possible. For each of the papers on these well-studied traits, we scored the trait-environment association as positive, negative, or not significant. We then synthesized the results to gain insight about the onset and duration of sensitive periods in that trait's development. Unfortunately, a meta-analysis of sensitive periods across trait modalities was not possible due to insufficient replication across life stages within taxa and the diversity of analysis techniques (e.g., PCA, model selection, and generalized linear mixed models) used to study the effects of environment on trait expression.

| RE SULTS
Our searches returned 869 unique papers ( Figure 1; Table S1). Of these, 123 (14%) met our criteria for inclusion in the summaries below. Selected papers were representative of the overall search Acoustic and visual traits in birds and visual, behavioral, and morphological traits in fish were the only traits for which all relevant life stages were studied (for many fish, there is no nonbreeding season), and thus, temporal patterns of plasticity (Table 2) could potentially be assessed only in these taxa.
All of our selected papers framed the trait(s) in question as a sexual signal, reproductive trait, or similar. However, the evidence given for sexual selection (i.e., a correlation with mate choice and/or reproductive success) was often weak or nonexistent. Over a third of the traits in selected papers were not clearly linked with mate choice or reproductive success (87/203 traits or 43%, total is greater than the number of selected papers because some papers studied multiple traits). In these cases, the authors either did not provide citations for statements describing a trait as sexually selected or provided indirect evidence (e.g., the trait is sexually dimorphic, linked with territory quality, or more common among dominant individuals). About half of the papers did cite evidence of the trait being linked with mate choice and/or reproductive success (99/203 traits or 49%), and a few exceptional papers directly tested the link with mate choice and/or reproductive success, as well as trait plasticity (17/203 or 8%; see Head et al., 2017;Martín & López, 2006 for good examples).

| Trait syntheses
The most well-represented species among selected papers were guppies (Poecilia reticulata, 14 papers), zebra finches (Taeniopygia guttata, 10 papers), three-spined sticklebacks (Gasterosteus aculeatus, seven papers), house sparrows (Passer domesticus, six papers), and great tits (Parus major, five papers). Together, these species represented over a third of the papers in our dataset. We identified four traits that met our criteria for further synthesis: song characteristics in zebra finches, sigmoid displays in guppies, orange coloration in guppies, and black badge size in house sparrows (see Methods; in brief, traits had to be (1) studied in multiple life stages, (2) sexually selected, and (3) measured consistently across studies). Below, we report what environment-trait associations have been found at different life stages and in response to different environmental variables for these traits. Furthermore, we integrate the results of different studies to highlight potential patterns of developmental, seasonal, or continuous plasticity in sexual trait development.

| Orange spot size in guppies
Guppies (Figure 5a) are live-bearing freshwater fish with a polyandrous mating system that has become a model system in sexual selection research. Male guppies display orange, yellow, white, black, and iridescent coloration in highly variable and individually unique patterns (Houde, 1997). The guppy's orange spots are carotenoidbased, a pigment known to be influenced by nutrition in many species as it cannot be synthesized by animals and must be acquired through the diet (Goodwin, 1984;Schiedt, 1989). The extent of orange coloration influences mate choice, with females preferring to mate with males who display more conspicuous orange coloration  (Endler, 1984;Kodric-Brown, 1985). For details on how genotypeby-environment interactions shape sexual selection in this species, see Kolluru (2014).
Our selected papers included seven studies that tested the effects of environmental variables on orange spot size (Table 3).
Environmental manipulations took place before and after sexual maturity (juvenile and breeding life stages, respectively). These studies did not all test the same environmental variables, but there is considerable overlap: Five studies manipulated some aspect of nutrition, likely because of the known physiological link between carotenoid pigmentation and diet. Four of these studies manipulated the quantity of food experimental fish received (Devigili et al., 2013;Evans et al., 2015;Rahman et al., 2013;Ruell et al., 2013), and two manipulated the carotenoid content of fish diets (Grether, 2000; F I G U R E 3 Summary of (a) number of traits, (b) trait modalities, (c) number of environmental variables, and (d) types of environmental variables considered in 123 papers that met our selection criteria. If a paper studied multiple types of traits or environmental variables, these were scored separately so the totals in (b) and (d) add to more than 123. "Other" environmental variables include water quality, preening effort, tail removal, previous reproductive effort, and administration of sex hormones   Rahman et al., 2013). The two remaining studies (Miller & Brooks, 2005;and Magris et al., 2018) tested the effects of the social environment (namely, the number and continued presence of females) but found no effect on orange coloration in either the juvenile or breeding stage.
Considering life stage (breeding or juvenile) helps explain when results of these studies agree or disagree with one another. The key is that inferences about trait plasticity from each study are limited to the time point in which the trait was analyzed and the environmental variable under consideration. When dietary manipulations took place during the juvenile stage, no association was found between carotenoid supplementation (Grether, 2000) or food quantity and orange spot size at maturity (Ruell et al., 2013). In contrast, when dietary manipulations took place after reaching sexual maturity (breeding), food quantity was positively associated with orange spot size (Devigili et al., 2013;Evans et al., 2015;Rahman et al., 2013).
This pattern indicates orange spot size may reflect environmental conditions experienced by male guppies at sexual maturity, but is not indicative of their early developmental environment, in accordance with a pattern of seasonal (breeding) plasticity (Table 2). Comparing the effects of nutritional manipulations with social manipulations highlights the point that a lack of evidence for trait plasticity is not evidence that a trait is not plastic. Rather, a trait may be sensitive to environmental variables and/or at life stages other than those being studied.

| Sigmoid displays of guppies
In addition to coloration, male guppies use a ritualized courtship behavior termed the "sigmoid display." This display is thought to show off a male's color patterns and display rates are linked with increased reproductive success (Houde, 1997).
Our selected papers included 11 papers that analyzed plasticity of sigmoid display rates at different life stages ( These studies provide mixed evidence for the effect of light levels during courtship (breeding) on display rates. Where some studies found no evidence of a correlation (Chapman et al., 2009;Kelley et al., 2013;Reynolds, 1993), others found that male guppies tended to display more in low light conditions (Kolluru et al., 2015) or high turbidity (Ehlman et al., 2018). Importantly, there is evidence that individual males may respond to lighting conditions differently depending on their rearing environment or size, as evidenced by a significant interaction with display rates (Chapman et al., 2009;Reynolds, 1993), and this individual variation may help to explain the apparent discrepancy between studies with similar methods.
The four studies testing social conditions did not all find evidence for a correlation with display rates, but these studies manipulated different aspects of social conditions. Neither female receptivity (Farr, 1980) nor variance in female size (Jordan & Brooks, 2012) was linked with display rates. The order and number of females present over a week did influence display rates, with sequential presentation of females resulting in higher display rates of male guppies (Jordan & Brooks, 2012). The one study that manipulated juvenile social conditions found that males who were allowed to court, but not mate with, females displayed more often than males housed separately from females or those who were allowed to mate with females (Miller & Brooks, 2005). This study manipulated social conditions continuously from before to after sexual maturity (juvenile and breeding), and therefore, it is not possible to determine whether display rates were sensitive to this manipulation before sexual maturity, afterward, or both.
Nutrition was only studied at one life stage (breeding), and across studies, food quantity was associated with increased display rates. Consistent with previous work that has established the continuous plasticity of behavioral traits (Table 2; Stamps, 2016), there is evidence that even very short-term changes in lighting, social Subjects were also exposed to mercury in ovo. b Significant interaction between rearing environment and display environment. c Significant interaction with size.

TA B L E 3 (Continued)
conditions, and nutrition can affect the display rates of male guppies; however, the evidence is somewhat mixed (

| Chest badge size in house sparrows
House sparrows (Figure 5b) are an extremely common, widespread songbird that have been studied extensively in aviaries and natural settings. They are sexually dimorphic, with males displaying a prominent black patch of feathers (badge or bib) on their throat and chest.
This patch is melanin-based, and the size of the patch has been associated with both inter-and intrasexual selection (Griffith et al., 1999b;Møller, 1988), although more recent meta-analyses point to a lack of evidence for sexual selection (Nakagawa et al., 2007;Sánchez-Tójar et al., 2018).
Included in our review were six studies that analyzed the environmental sensitivity of badge size at different life stages ( Table 3): Two of these studies were conducted on juvenile birds (Gonzalez et al., 1999;Griffith et al., 1999a) and one on nonbreeding birds (McGraw et al., 2002). None of these three studies found an effect of nutritional conditions on badge size.
In contrast, badge size increased with aggressive social conditions during molt (McGraw et al., 2003) and decreased with greater breeding effort in the prior breeding season (Griffith, 2000). Therefore, badge size is plastic during molt (nonbreeding) but is likely more sensitive to social environment and prior reproductive effort than to nutritional conditions. Taken together, these results are consistent with a pattern of seasonal plasticity during molt (Table 2), although it may be plastic at other time points as well.

| Syllable repertoire in zebra finches
Zebra finches (Figure 5c) are a small, socially monogamous songbird that have been used extensively in laboratory studies, mainly in studies of neural development. Zebra finches sing a complex, rhythmic song that is a multicomponent signal. High syllable repertoire is among the song traits preferred by females (for a detailed review of song function and sexual selection in zebra finches, see Riebel, 2009). Included in our review were six studies that analyzed syllable repertoire (also referred to as number of unique syllables or elements; Table 3).
Once again, considering life stage helps when interpreting these studies together. Four studies manipulated nutritional conditions, but only during the juvenile stage is there evidence for effects on syllable repertoire (Noguera et al., 2017;Woodgate et al., 2014).
Manipulations of food quantity during the breeding season did not affect syllable repertoire (Ritschard & Brumm, 2012), and exposure to mercury did not affect syllable repertoire, despite the treatment occurring across both juvenile and adult life stages (Greene et al., 2018). There is also evidence that social conditions during the juvenile environment (tutor identity and number of males in tutoring group) affect syllable repertoire, but these were not tested during the breeding season (Gil et al., 2006). In line with the well-known pattern of heightened neural plasticity in the song learning system during early development, that is, developmental plasticity (Table 2; Arnold, 1992;Larson, 2020), the juvenile developmental period is likely to be when this song trait is most environmentally sensitive.

| D ISCUSS I ON
In this review, we asked how timing, in addition to type of environmental variation, affects patterns of plasticity in sexual signal traits.
As shown in our synthesis of traits in guppies, zebra finches, and house sparrows, applying a temporal perspective on trait plasticity can help to integrate and reconcile results of different studies.
Without this perspective, these studies may seem to be in conflict with one another, with some providing evidence of trait plasticity and some finding no evidence of trait plasticity. Yet, in reality, traits may have differential sensitivity to their environment over time. In addition, these trait syntheses show how patterns of plasticity may differ among trait modalities, but we were unable to conduct a formal analysis due to the limitations of our dataset-namely, that most trait-environment associations were only tested in one life stage (e.g., all acoustic traits in amphibians were studied during the breeding season; Figure 4).

| The temporal nature of plasticity and the information conveyed by sexual traits
The time at which trait expression is sensitive to the environment varies among traits. Some traits are plastic only during early development (developmental plasticity), some traits are plastic at particular, recurrent times (seasonal plasticity), and yet other traits remain plastic throughout life (continuous plasticity, Table 2; Arnold, 1992;Stamps, 2016). In reality, of course, most sexual traits are influenced by a mixture of inherited genetic information and environmental influences that are experienced over an animal's life, and thus, most traits will resist strict categorization.
Nevertheless, identifying sensitive periods during which environmental exposure has the greatest impact on future trait expression is useful, as this provides important insights related to trait function and evolution (see Box 1).
Physiological knowledge of the trait in question is key to identifying likely periods of heightened plasticity. Many internal physiological mechanisms can mediate changes in trait expression following environmental changes, including oxidative stress (Hill, 2011), sex hormones (Bókony et al., 2008), stress hormones (San-Jose & Fitze, 2013), inflammatory immune responses (Saino et al., 2013), insulin signaling (Warren et al., 2013), and more. Epigenetic changes, for example, DNA methylation, may result from changes in internal physiological status, particularly when there is a delay between the sensitive period and eventual trait expression (Laubach et al., 2018).
The information conveyed by sexual traits is altered by the timing of plasticity of that trait (see Box 1), since expression of a plastic trait depends on not only what environmental influences the individual has experienced, but also when.

| Implications for population divergence
Both the type and timing of environmental exposure may modify the information conveyed by sexual traits on an individual level, and selection on this variation at the individual level scales to affect population outcomes. Sexual selection has been viewed as potentially important in speciation processes (Panhuis et al., 2001;Ritchie, 2007;Safran et al., 2013;Servedio & Boughman, 2017;reviewed in Lindsay et al., 2019). Further, there is growing evidence that the environmental context in which populations exist is likely to have broad implications for the evolution of divergent sexual selection (Maan & Seehausen, 2011;Safran et al., 2013). For example, a recent study of closely related populations of barn swallows shows that different parasite populations are associated with the most divergent aspects of sexually selected traits (Hund et al., 2020), suggesting an interactive role of sexual selection and environmental context (parasites, in this case) in the differentiation of phenotype. The role of plasticity is expected to modify the outcome of sexual selection (Cornwallis & Uller, 2010). Plasticity can dampen selection and thus maintain genetic diversity that is drawn from when populations are separated or begin to occupy new environments (Ingleby et al., 2010). Genotype-by-environment interactions in particular are increasingly studied in the context of sexual selection (Evans et al., 2015;Ingleby et al., 2010;Mills et al., 2007), an extremely valuable direction in helping to understand phenotypic variation and the divergence process. However, whether plasticity in sexual traits should accelerate or hinder divergence, and how population fitness may be affected, remains unclear (Fox et al., 2019). Key parameters likely include the degree to which environments differ, the degree of gene flow between populations (Ingleby et al., 2010), and sex differences in plasticity itself (Svensson et al., 2014). Despite increased interest in how plasticity affects sexual selection and divergence, the existence of sensitive periods in sexual traits is infrequently considered when studying how plasticity may modify evolutionary outcomes of sexual selection. Below, we consider how sensitive periods in plasticity of sexual traits may affect evolution and divergence, particularly in migratory or recently isolated populations.  (Irwin, 2009;Turbek et al., 2018). If the traits used in mate selection are seasonally plastic and develop in environmentally different overwintering locations, trait differences may become coupled with nonbreeding location ( Figure 6a). As such, when individuals arrive from different wintering locations they may return with increasingly different sexual traits that, when used in mate selection, may contribute to population divergence (Rolshausen et al., 2009). This is particularly true of "magic traits"-traits under divergent selection that also affect mate choice, such as breeding timing (Servedio et al., 2011). In contrast, if traits used in mate selection are seasonally plastic but develop in the shared breeding grounds, no environmentally relevant information about divergent migratory routes can be encoded in the sexual traits ( Figure 6b) and divergence would not be expected to occur via sexual signaling.

| Continuous plasticity
For traits that are continuously plastic, such as the sigmoid display of guppies, the dynamics of trait expression and changes in immediate environmental context are targets for study. Even with the same trait and preference, movement to a novel environment (e.g., with novel parasites or new food sources) may affect the expression, cost, or honesty of trait, creating new selection on preferences (Maan & Seehausen, 2011) and potentially allow the evolution of new environment-trait linkages (Hund et al., 2020). While large-scale environmental changes such as a warming climate are likely to affect all individuals in F I G U R E 6 Conceptual diagram illustrating scenarios in which seasonal trait plasticity may (a) contribute to divergence or (b) erode divergence in migratory populations that share breeding locations but occupy different nonbreeding locations (i.e., there is a migratory divide). In (a), the trait is plastic during the time when the two populations are in two different nonbreeding locations; therefore, the environment could potentially differentially affect trait expression leading to phenotypic differentiation between the two populations upon return to their shared breeding grounds. In (b), the trait is plastic during the time when the two populations occupy the same breeding location; therefore, the environment cannot differentially affect trait expression among the two populations

| CON CLUS ION
In this review, we screened over 850 papers, which were then filtered for data collection on plasticity in studies of sexually selected traits in vertebrates. Our summary of this literature revealed that the existence of sensitive periods has been overlooked in studies of phenotypic plasticity of sexual traits. Further, a detailed synthesis of the most well-studied traits ( Throughout, we outline patterns of plasticity that differ in when the environment affects trait expression. Although this temporal aspect of plasticity has been recognized for decades, there has been little empirical research on its implications for sexual selection. We advocate continued investigation into how plasticity shapes sexual selection, with particular attention to the timing of environmental interactions in altering animal physiology and expression of sexual traits. The timing of environment-trait interactions has important implications for trait evolution and population divergence.

ACK N OWLED G M ENTS
We thank members of the Safran Lab for feedback on early ideas, Libraries Open Access Fund.

CO N FLI C T O F I NTE R E S T
The authors declare that they have no conflicts of interest. Writing-review & editing (supporting).

DATA AVA I L A B I L I T Y S TAT E M E N T
All data used in this paper are from previously published and publicly available manuscripts listed in Table S1.