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.

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.

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.

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.

How moonlight shapes environments, life histories, and ecological interactions on coral reefs.

The lunar cycle drives variation in nocturnal brightness. For the epipelagic larvae of coral reef organisms, nocturnal illumination may have widespread and underappreciated consequences. At sea, the onset of darkness coincides with an influx of mesopelagic organisms to shallow water (i.e. 'diel vertical migrants') that include predators (e.g. lanternfishes) and prey (zooplankton) of zooplanktivorous coral reef larvae. Moonlight generally suppresses this influx, but lunar periodicity in the timing and intensity of nocturnal brightness may affect vertically migrating predators and prey differently. A major turnover of species occurs at sunset on the reef, with diurnal species seeking shelter and nocturnal species emerging to hunt. The hunting ability of nocturnal reef-based predators is aided by the light of the moon. Consequently, variation in nocturnal illumination is likely to shape the timing of reproduction, larval development, and settlement for many coral reef organisms. This synthesis underscores the potential importance of trophic linkages between coral reefs and adjacent pelagic ecosystems, facilitated by the diel migrations of mesopelagic organisms and the ontogenetic migrations of coral reef larvae. Research is needed to better understand the effects of lunar cycles on life-history strategies, and the potentially disruptive effects of light pollution, turbidity, and climate-driven changes to nocturnal cloud cover. These underappreciated threats may alter patterns of nocturnal illumination that have shaped the evolutionary history of many coral reef organisms, with consequences for larval survival and population replenishment that could rival or exceed other effects arising from climate change.

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.

Ejaculate Allocation and Sperm Characteristics Differ among Alternative Male Types in a Species of Fish with Cooperation and Competition among Unrelated Males.

Sexual selection arising from sperm competition has driven the evolution of immense variation in ejaculate allocation and sperm characteristics not only among species, but also among males within a species. One question that has received little attention is how cooperation among males affects these patterns. Here we ask how male alternative reproductive types differ in testes size, ejaculate production, and sperm morphology in the ocellated wrasse, a marine fish in which unrelated males cooperate and compete during reproduction. Nesting males build nests, court females and provide care. Sneaker males only "sneak" spawn, while satellite males sneak, but also help by chasing away sneakers. We found that satellite males have larger absolute testes than either sneakers or nesting males, despite their cooperative role. Nesting males invested relatively less in testes than either sneakers or satellites. Though sneakers produced smaller ejaculates than either satellite or nesting males, we found no difference among male types in either sperm cell concentration or sperm number, implying sneakers may produce less seminal fluid. Sperm tail length did not differ significantly among male types, but sneaker sperm cells had significantly larger heads than either satellite or nesting male sperm, consistent with past research showing sneakers produce slower sperm. Our results highlight that social interactions among males can influence sperm and ejaculate production.

Anti-racist interventions to transform ecology, evolution and conservation biology departments.

Racial and ethnic discrimination persist in science, technology, engineering and mathematics fields, including ecology, evolution and conservation biology (EECB) and related disciplines. Marginalization and oppression as a result of institutional and structural racism continue to create barriers to inclusion for Black people, Indigenous people and people of colour (BIPOC), and remnants of historic racist policies and pseudoscientific theories continue to plague these fields. Many academic EECB departments seek concrete ways to improve the climate and implement anti-racist policies in their teaching, training and research activities. We present a toolkit of evidence-based interventions for academic EECB departments to foster anti-racism in three areas: in the classroom; within research laboratories; and department wide. To spark restorative discussion and action in these areas, we summarize EECB's racist and ethnocentric histories, as well as current systemic problems that marginalize non-white groups. Finally, we present ways that EECB departments can collectively address shortcomings in equity and inclusion by implementing anti-racism, and provide a positive model for other departments and disciplines.

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.

Sperm and alternative reproductive tactics: a review of existing theory and empirical data.

Males that exhibit alternative reproductive tactics (ARTs) often differ in the risk of sperm competition and the energetic trade-offs they experience. The resulting patterns of selection could lead to between-tactic differences in ejaculate traits. Despite extensive research on male ARTs, there is no comprehensive review of whether and what differences in sperm traits exist between male ARTs. We review existing theory on ejaculate evolution relevant to ARTs and then conduct a comprehensive vote-counting review of the empirical data comparing sperm traits between males adopting ARTs. Despite the general expectation that sneaker males should produce sperm that are more competitive (e.g. higher quality or performance), we find that existing theory does not predict explicitly how males adopting ARTs should differ in sperm traits. The majority of studies find no significant difference in sperm performance traits between dominant and sneaker males. However, when there is a difference, sneaker males tend to have higher sperm performance trait values than dominant males. We propose ways that future theoretical and empirical research can improve our understanding of the evolution of ejaculate traits in ARTs. We then highlight how studying ejaculate traits in species with ARTs will improve our broader knowledge of ejaculate evolution. This article is part of the theme issue 'Fifty years of sperm competition'.

Reproductive phenology across the lunar cycle: parental decisions, offspring responses, and consequences for reef fish.

Most organisms reproduce in a dynamic environment, and life-history theory predicts that this can favor the evolution of strategies that capitalize on good times and avoid bad times. When offspring experience these environmental changes, fitness can depend strongly upon environmental conditions at birth and at later life stages. Consequently, fitness will be influenced by the reproductive decisions of parents (i.e., birth date effects) and developmental decisions (e.g., adaptive plasticity) of their offspring. We explored the consequences of these decisions using a highly iteroparous coral reef fish (the sixbar wrasse, Thalassoma hardwicke) and in a system where both parental and offspring environments vary with the lunar cycle. We tested the hypotheses that (1) reproductive patterns and offspring survival vary across the lunar cycle and (2) offspring exhibit adaptive plasticity in development time. We evaluated temporal variation in egg production from February to June 2017, and corresponding larval developmental histories (inferred from otolith microstructure) of successful settlers and surviving juveniles that were spawned during that same period. We documented lunar-cyclic variation in egg production (most eggs were spawned at the new moon). This pattern was at odds with the distribution of birth dates of settlers and surviving juveniles-most individuals that successfully survived to settlement and older stages were born during the full moon. Consequently, the probability of survival across the larval stage was greatest for offspring born close to the full moon, when egg production was at its lowest. Offspring also exhibited plasticity in developmental duration, adjusting their age at settlement to settle during darker portions of the lunar cycle than expected given their birth date. Offspring born near the new moon tended to be older and larger at settlement, and these traits conveyed a strong fitness advantage (i.e., a carryover effect) through to adulthood. We speculate that these effects (1) are shaped by a dynamic landscape of risk and reward determined by moonlight, which differentially influences adults and offspring, and (2) can explain the evolution of extreme iteroparity in sixbars.

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.

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.

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.

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.

Ovarian fluid allows directional cryptic female choice despite external fertilization.

In species with internal fertilization, females can favour certain males over others, not only before mating but also within the female's reproductive tract after mating. Here, we ask whether such directional post-mating (that is, cryptic) female mate choice can also occur in species with external fertilization. Using an in vitro sperm competition experiment, we demonstrate that female ovarian fluid (ovarian fluid) changes the outcome of sperm competition by decreasing the importance of sperm number thereby increasing the relative importance of sperm velocity. We further show that ovarian fluid does not differentially affect sperm from alternative male phenotypes, but generally enhances sperm velocity, motility, straightness and chemoattraction. Under natural conditions, female ovarian fluid likely increases the paternity of the preferred parental male phenotype, as these males release fewer but faster sperm. These results imply females have greater control over fertilization and potential to exert selection on males in species with external fertilization than previously thought possible.

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.