On the resolution of sexual conflict over shared traits.

Anisogamy, different-sized male and female gametes, sits at the heart of sexual selection and conflict between the sexes. Sperm producers (males) and egg producers (females) of the same species generally share most, if not all, of the same genome, but selection frequently favours different trait values in each sex for traits common to both. The extent to which this conflict might be resolved, and the potential mechanisms by which this can occur, have been widely debated. Here, we summarize recent findings and emphasize that once the sexes evolve, sexual selection is ongoing, and therefore new conflict is always possible. In addition, sexual conflict is largely a multivariate problem, involving trait combinations underpinned by networks of interconnected genes. Although these complexities can hinder conflict resolution, they also provide multiple possible routes to decouple male and female phenotypes and permit sex-specific evolution. Finally, we highlight difficulty in the study of sexual conflict over shared traits and promising directions for future research.

Lunar rhythms and their carry-over effects may shape environmental sex determination in a coral reef fish.

Lunar rhythms shape spawning phenology and subsequent risks and rewards for early life-history stages in the sea. Here, we consider a perplexing spawning phenology of the sixbar wrasse (Thalassoma hardwicke), in which parents spawn disproportionately around the new moon, despite the low survival of these larvae. Because primary sex determination in this system is highly plastic and sensitive to social environments experienced early in development, we ask whether this puzzling pattern of spawning is explained by fitness trade-offs associated with primary sexual maturation. We used otoliths from 871 fish to explore how spawning on different phases of the moon shapes the environments and phenotypes of settling larvae. Offspring that were born at the new moon were more likely to settle (i) before other larvae, (ii) at a larger body size, (iii) at an older age, (iv) to the best quality sites, and (v) as part of a social group-all increasing the likelihood of primary maturation to male. Selection of birthdates across life stage transitions suggests that the perplexing spawning phenology of adults may reflect an evolutionarily stable strategy that includes new moon spawning for compensatory benefits later in life, including preferential production of primary males at certain times.

Patterns of spawning and settlement of reef fishes as strategic responses to post-settlement competition.

Settlement is a critical transition in the life history of reef fish, and the timing of this event can have a strong effect on fitness. Key factors that influence settlement timing are predictable lunar cyclic variation in tidal currents, moonlight, and nocturnal predation risk as larvae transition from pelagic to benthic environments. However, populations typically display wide variation in the arrival of settlers over the lunar cycle. This variation is often hypothesized to result from unpredictable conditions in the pelagic environment and bet-hedging by spawning adults. Here, we consider the hypothesis that the timing of spawning and settlement is a strategic response to post-settlement competition. We use a game theoretic model to predict spawning and settlement distributions when fish face a tradeoff between minimizing density-independent predation risk while crossing the reef crest vs. avoiding high competitor density on settlement habitat. In general, we expect competition to spread spawning over time such that settlement is distributed around the lunar phase with the lowest predation risk, similar to an ideal free distribution in which competition spreads competitors across space. We examine the effects of overcompensating density dependence, age-dependent competition, and competition among daily settler cohorts. Our model predicts that even in the absence of stochastic variation in the larval environment, competition can result in qualitative divergence between spawning and settlement distributions. Furthermore, we show that if competitive strength increases with settler age, competition results in covariation between settler age and settlement date, with older larvae settling when predation risk is minimal. We predict that competition between daily cohorts delays peak settlement, with priority effects potentially selecting for a multimodal settlement distribution.

Learning from Our Study Organisms about Sexual Selection: Lessons from the Ocellated Wrasse.

AbstractSexual selection is a powerful force shaping not only the details but also the breadth of what we see in nature. Yet so much unexplained variation remains. Organisms often solve the "problem" of how to pass on their genes in ways that do not fit our current expectations. I argue here that integrating empirical surprises will push our understanding of sexual selection forward. Such "nonmodel" organisms (i.e., species that do not do what we think they should do) challenge us to think deeply, integrate puzzling results, question our assumptions, and consider the new (and arguably better) questions these unexpected patterns pose. In this article, I share how puzzling observations from my long-term research on the ocellated wrasse (Symphodus ocellatus) have shaped my understanding of sexual selection and suggested new questions about the interplay among sexual selection, plasticity, and social interactions. My general premise, however, is not that others should study these questions. Instead, I argue for a change in the culture of our field-to consider unexpected results a welcome opportunity to generate new questions and learn new things about sexual selection. Those of us in positions of power (e.g., as editors, reviewers, and authors) need to lead the way.

Social Environment Influences the Temporal Dynamics of Sneak-Spawning in a Fish with Alternative Reproductive Tactics.

AbstractSeveral predictions of sperm competition theory are not well supported empirically. One potential reason is that most current theory and empirical research ignore how the social environment influence the temporal dynamics of mating. We propose that understanding these dynamics is key to understanding sexual selection and improving the predictive power of theory. To demonstrate the importance of these dynamics, we quantify how males' social role, interactions among males, and current social environment influence the timing of mating in Symphodus ocellatus, a species with three alternative male reproductive tactics. Nesting males spawn synchronously with females; sneakers and satellites sneak-spawn with some time delay. Satellites also cooperate with nesting males. We found that satellites have shorter sneak-spawning delays than sneakers, a benefit of their cooperation with nesting males. Sneak-spawning delays decreased with increasing nest activity for sneakers but not for satellites, suggesting that sneakers may benefit from increased sperm competition intensity. Current sperm competition models ignore this potential benefit, which may be why the prediction that males should decrease investment when sperm competition involves more than two males is not well supported. Our study provides insight into mechanisms that drive variation in the timing of spawning, which could explain mismatches between theoretical and empirical results.

Life history, mating dynamics and the origin of parental care.

Parental care, mating dynamics and life history co-evolve. Understanding the diversity of reproductive patterns found in nature is a major focus of evolutionary ecology research. Previous research suggests that the origin of parental care of eggs will be favoured when egg and adult death rates and juvenile survival are relatively high. However, the previous research that explored the link between care and life history did not account for among-species variation in mating dynamics. As mating dynamics are generally expected to influence care, we explore, theoretically, the life-history conditions (stage-specific rates of maturation and survival) that favour parental care across three mating scenarios: reproductive rate (1) is unaffected by males (assuming that some males are present), (2) increases as male abundance increases or (3) decreases as male abundance increases. Across scenarios, all forms of care were most strongly favoured when egg and adult death rates, juvenile survival and female egg maturation rates were relatively high. When reproductive rate was unaffected by male abundance or increased as male abundance increased, as we might expect in systems in which females are mate-limited, all forms of care were most strongly favoured when male egg maturation rate (i.e. the rate at which male eggs develop, mature and hatch) was moderate or high. When greater male abundance inhibited reproduction, which might occur in systems with intense male-male competition, all forms of care were most strongly favoured when male egg maturation rate was low-to-moderate. These results suggest that life history affects the evolution of parental care, and sex-specific life history can interact with mating dynamics to influence the origin of care.

Multispecies colour polymorphisms associated with contrasting microhabitats in two Mediterranean wrasse radiations.

Intraspecific colour polymorphisms (CPs) present unique opportunities to study fundamental evolutionary questions, such as the link between ecology and phenotype, mechanisms maintaining genetic diversity and their putative role in speciation. Wrasses are highly diverse in ecology and morphology and harbour a variety of colour-polymorphic species. In the Mediterranean Sea, wrasses of the tribe Labrini evolved two species radiations each harbouring several species with a brown and a green morph. The colour morphs occur in complete sympatry in mosaic habitats with rocky outcrops and Neptune grass patches. Morph-specific differences had not been characterized yet and the evolutionary forces maintaining them remained unknown. With genome-wide data for almost all Labrini species, we show that species with CPs are distributed across the phylogeny, but show evidence of hybridization. This suggests that the colour morphs are either ancient and have been lost repeatedly, that they have evolved repeatedly or have been shared via hybridization. Focusing on two polymorphic species, we find that each colour morph is more common in the microhabitat providing the best colour match and that the morphs exhibit additional behavioural and morphological differences further improving crypsis in their respective microhabitats. We find little evidence for genetic differentiation between the morphs in either species. Therefore, we propose that these colour morphs represent a multi-niche polymorphism as an adaptation to the highly heterogeneous habitat. Our study highlights how colour polymorphism (CP) can be advantageous in mosaic habitats and that Mediterranean wrasses are an ideal system to study trans-species polymorphisms, i.e. polymorphisms maintained across several species, in adaptive radiations.

Lunar rhythms in growth of larval fish.

Growth and survival of larval fishes is highly variable and unpredictable. Our limited understanding of this variation constrains our ability to forecast population dynamics and effectively manage fisheries. Here we show that daily growth rates of a coral reef fish (the sixbar wrasse, Thalassoma hardwicke) are strongly lunar-periodic and predicted by the timing of nocturnal brightness: growth was maximized when the first half of the night was dark and the second half of the night was bright. Cloud cover that obscured moonlight facilitated a 'natural experiment', and confirmed the effect of moonlight on growth. We suggest that lunar-periodic growth may be attributable to light-mediated suppression of diel vertical migrations of predators and prey. Accounting for such effects will improve our capacity to predict the future dynamics of marine populations, especially in response to climate-driven changes in nocturnal cloud cover and intensification of artificial light, which could lead to population declines by reducing larval survival and growth.

An escape theory model for directionally moving prey and an experimental test in juvenile Chinook salmon.

Prey evaluate risk and make decisions based on the balance between the costs of predation and those of engaging in antipredator behaviour. Economic escape theory has been valuable in understanding the responses of stationary prey under predation risk; however, current models are not applicable for directionally moving prey. Here we present an extension of existing escape theory that predicts how much predation risk is perceived by directionally moving prey. Perceived risk is measured by the extent antipredator behaviour causes a change in travel speed (the distance to a destination divided by the total time to reach that destination). Cryptic or cautious antipredator behaviour slows travel speed, while prey may also speed up to reduce predator-prey overlap. Next, we applied the sensitization hypothesis to our model, which predicts that prey with more predator experience should engage in more antipredator behaviour, which leads to a larger change in travel speed under predation risk. We then compared the qualitative predictions of our model to the results of a behavioural assay with juvenile Chinook salmon Oncorhynchus tshawytscha that varied in their past predator experience. We timed salmon swimming downstream through a mesh enclosure in the river with and without predator cues present to measure their reaction to a predator. Hatchery salmon had the least predator experience, followed by wild salmon captured upstream (wild-upstream) and wild-salmon captured downstream (wild-downstream). Both wild salmon groups slowed down in response to predator cues, whereas hatchery salmon did not change travel speed. The magnitude of reaction to predator cues by salmon group followed the gradient of previous predator experience, supporting the sensitization hypothesis. Moving animals are conspicuous and vulnerable to predators. Here we provide a novel conceptual framework for understanding how directionally moving prey perceive risk and make antipredator decisions. Our study extends the scope of economic escape theory and improves general understanding of non-lethal effects of predators on moving prey.

Grey zones of sexual selection: why is finding a modern definition so hard?

Sexual selection has long been acknowledged as an important evolutionary force, capable of shaping phenotypes ranging from fascinating and unusual displays to cryptic traits whose function is only uncovered by careful study. Yet, despite decades of research, reaching a consensus definition of the term 'sexual selection' has proved difficult. Here we explore why arriving at a unifying definition of sexual selection is so hard. While some researchers have argued about whether sexual selection should be considered a form of natural selection, we concentrate on where the line between sexual selection and other forms of selection falls. We focus on identifying the 'grey zones' of sexual selection by illustrating cases in which application of the term 'sexual selection' would be considered controversial or ambiguous. We believe that clarifying why sexual selection is so difficult to define is an essential first step forward towards greater clarity, and if possible towards reaching a consensus definition. We suggest that a more nuanced perspective may be necessary, particularly one that specifies for cases of 'sexual selection' why the term is used or whether they fall into a grey zone.

Experimentally induced variation in neuroendocrine processes affects male reproductive behaviour, sperm characteristics and social interactions.

While extensive research has focused on how social interactions evolve, the fitness consequences of the neuroendocrine mechanisms underlying these interactions have rarely been documented, especially in the wild. Here, we measure how the neuroendocrine mechanisms underlying male behaviour affect mating success and sperm competition in the ocellated wrasse (Symphodus ocellatus). In this species, males exhibit three alternative reproductive types. "Nesting males" provide parental care, defend territories and form cooperative associations with unrelated "satellites," who cheat by sneaking fertilizations but help by reducing sperm competition from "sneakers" who do not cooperate or provide care. To measure the fitness consequences of the mechanisms underlying these social interactions, we used "phenotypic engineering" that involved administering an androgen receptor antagonist (flutamide) to wild, free-living fish. Nesting males treated with flutamide shifted their aggression from sneakers to satellite males and experienced decreased submissiveness by sneaker males (which correlated with decreased nesting male mating success). The preoptic area (POA), a region controlling male reproductive behaviours, exhibited dramatic down-regulation of androgen receptor (AR) and vasotocin 1a receptor (V1aR) mRNA following experimental manipulation of androgen signalling. We did not find a direct effect of the manipulation on male mating success, paternity or larval production. However, variation in neuroendocrine mechanisms generated by the experimental manipulation was significantly correlated with changes in behaviour and mating success: V1aR expression was negatively correlated with satellite-directed aggression, and expression of its ligand arginine vasotocin (AVT) was positively correlated with courtship and mating success, thus revealing the potential for sexual selection on these mechanisms.

Female resistance to sexual coercion can evolve to preserve the indirect benefits of mate choice.

Sexual conflict over the indirect benefits of mate choice may arise when traits in one sex limit the ability of the other sex to freely choose mates but when these coercive traits are not necessarily directly harmful (i.e. forced fertilization per se). Although we might hypothesize that females can evolve resistance in order to retain the indirect, genetic benefits (reflected in offspring attractiveness) of mating with attractive males, up to now it has been difficult to evaluate potential underlying mechanisms. Traditional theoretical approaches do not usually conceptually distinguish between female preference for male mating display and female resistance to forced fertilization, yet sexual conflict over indirect benefits implies the simultaneous action of all of these traits. Here, we present an integrative theoretical framework that draws together concepts from both sexual selection and sexual conflict traditions, allowing for the simultaneous coevolution of displays and preferences, and of coercion and resistance. We demonstrate that it is possible for resistance to coercion to evolve in the absence of direct costs of mating to preserve the indirect benefits of mate choice. We find that resistance traits that improve the efficacy of female mating preference can evolve as long as females are able to attain some indirect benefits of mating with attractive males, even when both attractive and unattractive males can coerce. These results reveal new evolutionary outcomes that were not predicted by prior theories of indirect benefits or sexual conflict.

Intentional multiple mating by females in a species where sneak fertilization circumvents female choice for parental males.

This paper describes how individual female ocellated wrasse Symphodus ocellatus distribute their spawning among males and nests in space and time. It is based on previously collected genetic data of larvae from ten different nests (used to reconstruct half and full-sibling groupings both within and among nests on multiple days) and behavioural data of marked females across the reproductive season. Both the genetic analyses and behavioural observations confirm that female S. ocellatus intentionally engage in multiple mating, by repeatedly spawning at the same nest on different days and at several different nests (up to 12 spawning events over 3 weeks), leading to mixed paternity among her young. The main benefit of such high and intentional multiple mating is probably insurance against brood failure due to nest predation, desertion or poor paternal care by the male. These findings reveal that even in systems where females attempt to avoid male-controlled mixed paternity, they may still engage in intentional multiple mating due to these potential benefits.

Sperm competition games when males invest in paternal care.

Sperm competition games investigate how males partition limited resources between pre- and post-copulatory competition. Although extensive research has explored how various aspects of mating systems affect this allocation, male allocation between mating, fertilization and parental effort has not previously been considered. Yet, paternal care can be energetically expensive and males are generally predicted to adjust their parental effort in response to expected paternity. Here, we incorporate parental effort into sperm competition games, particularly exploring how the relationship between paternal care and offspring survival affects sperm competition and the relationship between paternity and paternal care. Our results support existing expectations that (i) fertilization effort should increase with female promiscuity and (ii) paternal care should increase with expected paternity. However, our analyses also reveal that the cost of male care can drive the strength of these patterns. When paternal behaviour is energetically costly, increased allocation to parental effort constrains allocation to fertilization effort. As paternal care becomes less costly, the association between paternity and paternal care weakens and may even be absent. By explicitly considering variation in sperm competition and the cost of male care, our model provides an integrative framework for predicting the interaction between paternal care and patterns of paternity.

Sperm competition shapes gene expression and sequence evolution in the ocellated wrasse.

Gene expression differences between males and females often underlie sexually dimorphic phenotypes, and the expression levels of genes that are differentially expressed between the sexes are thought to respond to sexual selection. Most studies on the transcriptomic response to sexual selection treat sexual selection as a single force, but postmating sexual selection in particular is expected to specifically target gonadal tissue. The three male morphs of the ocellated wrasse (Symphodus ocellatus) make it possible to test the role of postmating sexual selection in shaping the gonadal transcriptome. Nesting males hold territories and have the highest reproductive success, yet we detected feminization of their gonadal gene expression compared to satellite males. Satellite males are less brightly coloured and experience more intense sperm competition than nesting males. In line with postmating sexual selection affecting gonadal gene expression, we detected a more masculinized expression profile in satellites. Sneakers are the lowest quality males and showed both de-masculinization and de-feminization of gene expression. We also detected higher rates of gene sequence evolution of male-biased genes compared to unbiased genes, which could at least in part be explained by positive selection. Together, these results reveal the potential for postmating sexual selection to drive higher rates of gene sequence evolution and shape the gonadal transcriptome profile.

Ocean acidification affects fish spawning but not paternity at CO2 seeps.

Fish exhibit impaired sensory function and altered behaviour at levels of ocean acidification expected to occur owing to anthropogenic carbon dioxide emissions during this century. We provide the first evidence of the effects of ocean acidification on reproductive behaviour of fish in the wild. Satellite and sneaker male ocellated wrasse (Symphodus ocellatus) compete to fertilize eggs guarded by dominant nesting males. Key mating behaviours such as dominant male courtship and nest defence did not differ between sites with ambient versus elevated CO2 concentrations. Dominant males did, however, experience significantly lower rates of pair spawning at elevated CO2 levels. Despite the higher risk of sperm competition found at elevated CO2, we also found a trend of lower satellite and sneaker male paternity at elevated CO2 Given the importance of fish for food security and ecosystem stability, this study highlights the need for targeted research into the effects of rising CO2 levels on patterns of reproduction in wild fish.

Why do cuckolded males provide paternal care?

In most species, males do not abandon offspring or reduce paternal care when they are cuckolded by other males. This apparent lack of adjustment of paternal investment with the likelihood of paternity presents a potential challenge to our understanding of what drives selection for paternal care. In a comparative analysis across birds, fish, mammals, and insects we identify key factors that explain why cuckolded males in many species do not reduce paternal care. Specifically, we show that cuckolded males only reduce paternal investment if both the costs of caring are relatively high and there is a high risk of cuckoldry. Under these circumstances, selection is expected to favour males that reduce paternal effort in response to cuckoldry. In many species, however, these conditions are not satisfied and tolerant males have outcompeted males that abandon young.

Females allocate differentially to offspring size and number in response to male effects on female and offspring fitness.

Female investment in offspring size and number has been observed to vary with the phenotype of their mate across diverse taxa. Recent theory motivated by these intriguing empirical patterns predicted both positive (differential allocation) and negative (reproductive compensation) effects of mating with a preferred male on female investment. These predictions, however, focused on total reproductive effort and did not distinguish between a response in offspring size and clutch size. Here, we model how specific paternal effects on fitness affect maternal allocation to offspring size and number. The specific mechanism by which males affect the fitness of females or their offspring determines whether and how females allocated differentially. Offspring size is predicted to increase when males benefit offspring survival, but decrease when males increase offspring growth rate. Clutch size is predicted to increase when males contribute to female resources (e.g. with a nuptial gift) and when males increase offspring growth rate. The predicted direction and magnitude of female responses vary with female age, but only when per-offspring paternal benefits decline with clutch size. We conclude that considering specific paternal effects on fitness in the context of maternal life-history trade-offs can help explain mixed empirical patterns of differential allocation and reproductive compensation.

Does the risk of sperm competition help explain cooperation between reproductive competitors? A study in the ocellated wrasse (Symphodus ocellatus).

Although cooperating individuals may gain benefits, they risk being cheated by their allies. Therefore, to understand the persistence of cooperation by mutual benefits, it is important to document both the potential benefits of cooperation and the risks of cheating. We experimentally examined evidence of cooperation in the ocellated wrasse (Symphodus ocellatus), a fish species with males that exercise three reproductive strategies: satellite and sneaker males attempt to parasitically spawn in the nests of nesting males. Nesting males have been hypothesized to tolerate satellites as a result of satellite aid in defense against sneaker males and help in courting females. Here, we provide evidence that cooperation between reproductive competitors may arise in response to sperm competition from other males. After we experimentally removed satellites, nesting males had more sneakers at their nest and experienced a higher rate of sneaking when they spawned (increased sperm competition risk). When we experimentally distracted nesting males to prevent their acting aggressively toward satellites, satellites spawned with females and ate eggs in the nest. Our results suggest that nesting males and satellites gain fitness benefits of reduced direct reproductive and sperm competition through cooperation. However, nesting males risk losing paternity, while satellites experience increased aggression and must invest in aggression themselves (i.e., they act aggressively toward sneakers).

The coevolutionary dynamics of cryptic female choice.

In contrast to sexual selection on traits that affect interactions between the sexes before mating, little theoretical research has focused on the coevolution of postmating traits via cryptic female choice (when females bias fertilization toward specific males). We used simulation models to ask (a) whether and, if so, how nondirectional cryptic female choice (female-by-male interactions in fertilization success) causes deviations from models that focus exclusively on male-mediated postmating processes, and (b) how the risk of sperm competition, the strength of cryptic female choice, and tradeoffs between sperm number and sperm traits interact to influence the coevolutionary dynamics between cryptic female choice and sperm traits. We found that incorporating cryptic female choice can result in males investing much less in their ejaculates than predicted by models with sperm competition only. We also found that cryptic female choice resulted in the evolution of genetic correlations between cryptic female choice and sperm traits, even when the strength of cryptic female choice was weak, and the risk of sperm competition was low. This suggests that cryptic female choice may be important even in systems with low multiple mating. These genetic correlations increased with the risk of sperm competition and as the strength of cryptic female choice increased. When the strength of cryptic female choice and risk of sperm competition was high, extreme codivergence of sperm traits and cryptic female choice preference occurred even when the sperm trait traded off with sperm number. We also found that male traits lagged behind the evolution of female traits; this lag decreased with increasing strength of cryptic female choice and risk of sperm competition. Overall, our results suggest that cryptic female choice deserves more attention theoretically and may be driving trait evolution in ways just beginning to be explored.