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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.

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.

Patterns of reproduction, such as size-fecundity relationships used in models to assess fish populations, are generally treated as static through time and invariant to environmental change. However, growing evidence suggests that changes in ocean conditions, such as warming water temperatures and reduced primary productivity, affect life history traits, including reproduction. Under controlled experimental conditions, we documented reproductive plasticity in the live-bearing rosy rockfish Sebastes rosaceus in response to different temperature and feeding regimes, with maternal size as a covariate. Rosy rockfish occur throughout the California Current, a highly dynamic ecosystem for which increased environmental variability is predicted with climate change. Females produced 0-5 larval broods annually. Larger females had disproportionately higher fecundity than smaller females by producing larger-sized broods and a greater number of annual broods. Warmer water temperature decreased the time interval between brood releases, likely reflecting faster egg and larval development. However, warmer temperature did not increase the total number of broods, potentially reflecting a tradeoff with increased metabolic demand. Well-fed females had better body condition and higher annual fecundity compared to poorly fed females, primarily due to a greater number of broods. Conversely, females with poor body condition at the start of the reproductive season did not reproduce, providing possible evidence of delayed maturation at smaller sizes or skipped spawning at larger sizes. Reproductive plasticity (in terms of whether and how many broods are produced per year) in response to the environment likely contributes to high inter-annual variation in population larval production. Understanding the causes and consequences of reproductive plasticity is critical to developing sustainable management strategies and predicting population response to changing climate conditions.

Asymmetries in power (the ability to influence the outcome of conflict) are ubiquitous in social interactions because interacting individuals are rarely identical. It is well documented that asymmetries in power influence the outcome of reproductive conflict in social groups. Yet power asymmetries have received little attention in the context of negotiations between caring parents, which is surprising given that parents are often markedly different in size. Here we built on an existing negotiation model to examine how power and punishment influence negotiations over care. We incorporated power asymmetry by allowing the more-powerful parent, rank 1, to inflict punishment on the less-powerful parent, rank 2. We then determined when punishment will be favored by selection and how it would affect the negotiated behavioral response of each parent. We found that with power and punishment, a reduction in one parent’s effort results in partial compensation by the other parent. However, the degree of compensation is asymmetric: the rank 2 compensates more than the rank 1. As a result, the fitness of rank 1 increases and the fitness of rank 2 decreases, relative to the original negotiation model. Furthermore, because power and punishment enable one parent to extract greater effort from the other, offspring can do better, that is, receive more total effort, when there is power and punishment involved in negotiations over care. These results reveal how power and punishment alter the outcome of conflict between parents and affect offspring, providing insights into the evolutionary consequences of exerting power in negotiations.

Uncovering the genetic, physiological, and developmental mechanisms underlying phenotypic variation is necessary for understanding how genetic and genomic variation shape phenotypic variation and for discovering possible targets of selection. Although the neural and endocrine mechanisms underlying social behavior are evolutionarily ancient, we lack an understanding of the proximate causes and evolutionary consequences of variation in these mechanisms. Here, we examine in the natural environment the behavioral, neuromolecular, and fitness consequences of a morpholino-mediated knockdown of the mineralocorticoid receptor (MR) in the brain of nesting males of the ocellated wrasse, Symphodus ocellatus, a species with male alternative reproductive tactics. Even though MR knockdown did not significantly change male behavior directly, this experimental manipulation strongly altered glucocorticoid signaling and neuroplasticity in the preoptic area, the putative hippocampus homolog, and the putative basolateral amygdala homolog. We also found that individual variation in stress axis gene expression and neuroplasticity is strongly associated with variation in male behavior and fitness-related traits. The brain region-specific effects of MR knockdown on phenotypic integration in the wild reported here suggest specific neuroendocrine and neuroplasticity pathways that may be targets of selection.

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.

Male–male competition is a well-known driver of reproductive success and sexually selected traits in many species. However, in some species, males work together to court females or defend territories against male competitors. Dominant (nesting) males sire most offspring, but subordinate (satellite) males are better able to obtain fertilizations relative to unpartnered males. Because satellites only gain reproductive success by sneaking, there has been much interest in identifying the mechanisms enforcing satellite cooperation (defense) and reducing satellite sneaking. One such potential mechanism is outside competition: unpartnered satellites can destabilize established male partnerships and may force partnered satellites to restrain from cheating to prevent the dominant male from replacing them with an unpartnered satellite. Here, we manipulated perceived competition in the Mediterranean fish Symphodus ocellatus by presenting an “intruding” satellite male to established nesting and satellite male pairs. Focal satellite aggression to the intruder was higher when focal satellites were less cooperative, suggesting that satellites increase aggression to outside competitors when their social position is less stable. In contrast, nesting male aggression to the intruder satellite increased as spawning activity increased, suggesting that nesting males increase their defense toward outside competitors when their current relationship is productive. We found no evidence of altered spawning activity or nesting/satellite male interactions before and after the presentation. These results collectively suggest that response to outside competition is directly linked to behavioral dynamics between unrelated male partners and may be linked to conflict and cooperation in ways that are similar to group-living species.

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.

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.

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.

© 2017 by the Ecological Society of America Parents are expected to make decisions about reproductive timing and investment that maximize their own fitness, even if this does not maximize the fitness of each individual offspring. When offspring survival is uncertain, selection typically favors iteroparity, which means that offspring born at some times can be disadvantaged, while others get lucky. The eventual fate of offspring may be further modified by their own decisions. Are fates of offspring set by birthdates (i.e., determined by parents), or can offspring improve upon the cards they've been dealt? If so, do we see adaptive plasticity in the developmental timing of offspring? We evaluate these questions for a coral reef fish (the sixbar wrasse, Thalassoma hardwicke) that is characterized by extreme iteroparity and flexible larval development. Specifically, we monitored larval settlement to 192 small reefs over 11 lunar months and found that most fish settled during new moons of a lunar cycle (consistent with preferential settlement on dark nights). Settlement was significantly lower than expected by chance during the full moon and last quarter of the lunar cycle (consistent with avoidance of bright nights). Survival after settlement was greatest for fish that settled during times of decreasing lunar illumination (from last quarter to new moon). Fish that settled on the last quarter of the lunar cycle were ~10% larger than fish that settled during other periods, suggesting larvae delay settlement to avoid the full moon. These results are consistent with a numerical model that predicts plasticity in larval development time that enables avoidance of settlement during bright periods. Collectively, our results suggest that fish with inauspicious birthdates may alter their developmental trajectories to settle at better times. We speculate that such interactions between parent and offspring strategies may reinforce the evolution of extreme iteroparity and drive population dynamics, by increasing the survival of offspring born at the “wrong” time by allowing them to avoid the riskiest times of settlement.

Size-based harvest limits or gear regulations are often used to manage fishing mortality and ensure the spawning biomass of females is sufficiently protected. Yet, management interactions with species’ mating systems that affect fishery sustainability and yield are rarely considered. For species with obligate male care, it is possible that size-specific harvest of males will decrease larval production. In order to examine how size-based management practices interact with mating systems, we modeled fisheries of two species with obligate care of nests, corkwing wrasse (Symphodus melops, Labridae) and lingcod (Ophiodon elongatus, Hexigrammidae) under two management scenarios, a minimum size limit and a harvest slot limit. We simulated the population dynamics, larval production, and yield to the fishery under a range of fishing mortalities. We also modeled size-dependent male care to determine its interaction with management. In both species, the slot limit decreased yield by less than 12% (relative to minimum size limits) at low fishing mortalities; at higher mortalities, individuals rarely survived to outgrow the slot and spawning potential decreased substantially relative to unfished levels, similar to minimum size limits. Spawning potential decreased less when managed with a slot limit if we included a positive feedback between male size, care, and hatching success, but the benefit of implementing the slot depended both on the relative proportions of each sex selected by the fishery, and on our assumptions regarding male size and care. This work highlights that the effects of size- and sex-selective fisheries management can be nuanced and produce counter-intuitive results.

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.

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.

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.

The presence of a predator can result in the alteration, loss or reversal of a mating preference. Under predation risk, females often change their initial preference for conspicuous males, favouring less flashy males to reduce the risk of being detected by predators. Previous studies on predator-induced plasticity in mate preferences have given females a choice between more and less conspicuous conspecific males. However, in species that naturally hybridize, it is also possible that females might choose an inconspicuous heterospecific male over a conspicuous conspecific male under predation risk. Our study addresses this question using the green swordtail (Xiphophorus helleri) and the southern platyfish (Xiphophorus maculatus), which are sympatric in the wild. We hypothesized that X. helleri females would prefer the sworded conspecific males in the absence of a predator but favour the less conspicuous, swordless, heterospecific males in the presence of a predator. Contrary to our expectation, females associated more with the heterospecific male than the conspecific male in the control (no predator) treatment, and they were non-choosy in the predator treatment. This might reflect that females were attracted to the novel male phenotype when there was no risk of predation but became more neophobic after predator exposure. Regardless of the underlying mechanism, our results suggest that predation pressure may affect female preferences for conspecific versus heterospecific males. We also found striking within-population, between-individual variation in behavioural plasticity: females differed in the strength and direction of their preferences, as well as in the extent to which they altered their preferences in response to changes in perceived predation risk. Such variation in female preferences for heterospecific males could potentially lead to temporal and spatial variation in hybridization rates in the wild.

The molecular mechanisms underlying phenotypic plasticity are not well understood. Identifying mechanisms underlying alternative reproductive tactics (ARTs) in species for which the behavioral and fitness consequences of this variation are well-characterized provides an opportunity to integrate evolutionary and mechanistic understanding of the maintenance of variation within populations. In the ocellated wrasse Symphodus ocellatus, the behavioral phenotypes of three distinct male morphs (sneakers, satellites, nesting males), which arise from a single genome, have been thoroughly characterized. To determine the neuroendocrine and genomic mechanisms associated with discrete phenotypic variation and ARTs in S. ocellatus in their natural environment, we constructed a whole brain de novo transcriptome and compared global patterns of gene expression between sexes and male morphs. Next we quantified circulating cortisol and 11-ketotestosterone (11-kt), mediators of male reproductive behaviors, as well as stress and gonadal steroid hormone receptor expression in the preoptic area (POA), ventral subpallial division of the telencephalon (VS), and dorsolateral telencephalon (DL), critical brain regions for social and reproductive behaviors. We found higher levels of 11-kt in nesting males and higher levels of cortisol in sneaker males relative to other male morphs and females. We also identified distinct patterns of brain-region specific hormone receptor expression between males such that most hormone receptors are more highly expressed in satellites and nesting males relative to sneakers and females. Our results establish the neuroendocrine and molecular mechanisms that underlie ARTs in the wild and provide a foundation for experimentally testing hypotheses about the relationship between neuromolecular processes and reproductive success. This article is protected by copyright. All rights reserved.

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’.

Although phenotypic variation within and among individuals in the same population may represent ‘noise’, it can also be the adaptive plasticity that allows organisms to adjust to varying environments or the heritable variation that fuels evolutionary change. Behavioral variation arises from a complex combination of adaptive and non-adaptive individual plasticity and consistency. Differentiating these sources of behavioral variation will require an integrated combination of evolutionary and mechanistic understanding. Yet, this integration comes with a variety of challenges. Here I argue that we will need concrete a priori predictions to make sense of the large and complex datasets this integration will require.

We thank the Editor and the anonymous referees for helpful comments and the Leverhulme Trust, NERC and the Royal Society for funding.

Sperm competition theory has traditionally focused on how male allocation responds to female promiscuity, when males compete to fertilize a single clutch of eggs. Here, we develop a model to ask how female sperm use and storage across consecutive reproductive events affect male ejaculate allocation and patterns of mating and paternity. In our model, sperm use (a single parameter under female control) is the main determinant of sperm competition, which alters the effect of female promiscuity on male success and, ultimately, male reproductive allocation. Our theory reproduces the general pattern predicted by existing theory that increased sperm competition favors increased allocation to ejaculates. However, our model predicts a negative correlation between male ejaculate allocation and female promiscuity, challenging the generality of a prevailing expectation of sperm competition theory. Early models assumed that the energetic costs of precopulatory competition and the level of sperm competition are both determined by female promiscuity, which leads to an assumed covariation between these two processes. By modeling precopulatory costs and sperm competition independently, our theoretical framework allows us to examine how male allocation should respond independently to variation in sperm competition and energetic trade-offs in mating systems that have been overlooked in the past.

Discrete variation in reproductive behavior and physiology is observed in diverse taxa. Although it is known that most within-sex alternative reproductive tactics arise as a consequence of phenotypic plasticity, relatively little is known about differential neural gene expression among plastic alternative reproductive phenotypes. In the ocellated wrasse Symphodus ocellatus, males exhibit one of three alternative tactics (nesting, satellite, and sneaker) within a reproductive season, but switch tactics between years. Satellites and sneakers spawn parasitically in dominant (nesting) males’ nests, but only nesting males provide parental care. Nesting and satellite males show transient cooperative defense of nests against sneakers. Here, we analyze circulating sex steroid hormone levels and neural gene expression profiles in these three male phenotypes and in females. 11-ketotestosterone (but not testosterone) was highest in nesting males, while estradiol was highest in females. Brain transcriptomes of satellites and females were most similar to each other and intermediate to nesting and sneaker males. Sneakers showed more total expression differences, whereas nesting males showed higher magnitude expression differences. Our findings reveal the surprising extent to which neural gene expression patterns vary across reproductive tactics that vary in a number of social traits, including aggression, territoriality, and cooperation, providing important insights into the molecular mechanisms that may underlie variation in cooperative and reproductive behavior.

Sex differences in parental care are thought to arise from differential selection on the sexes. Sexual dimorphism, including sexual size dimorphism (SSD), is often used as a proxy for sexual selection on males. Some studies have found an association between male-biased SSD (i.e., males larger than females) and the loss of paternal care. While the relationship between sexual selection on males and parental care evolution has been studied extensively, the relationship between female-biased SSD (i.e., females larger than males) and the evolution of parental care has received very little attention. Thus, we have little knowledge of whether female-biased SSD coevolves with parental care. In species displaying female-biased SSD, we might expect dimorphism to be associated with the evolution of paternal care or perhaps the loss of maternal care. Here, drawing on data for 99 extant frog species, we use comparative methods to evaluate how parental care and female-biased SSD have evolved over time. Generally, we find no significant correlation between the evolution of parental care and female-biased SSD in frogs. This suggests that differential selection on body size between the sexes is unlikely to have driven the evolution of parental care in these clades and questions whether we should expect sexual dimorphism to exhibit a general relationship with the evolution of sex differences in parental care.

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.

To inquire how male size interacts with alloparental behaviour and mating success in the tessellated darter Etheostoma olmstedi, males were given a choice of nests with or without eggs; subsequent nest occupancy, takeovers and egg deposits were monitored. Subordinate males readily occupied available nests with eggs but were often evicted by dominant males, suggesting that males of all sizes compete for the opportunity to provide allopaternal care in this species.

Correlations between male phenotype and female investment in offspring size or number may result from either male influences or female responses to male phenotype. Theory has predicted that females may invest differentially in response to mate attractiveness either to take advantage of her partner’s attractiveness or to compensate for it. The outcome can depend on the female’s expected future fitness. Empirical evidence also suggests that females adjust offspring size or fecundity according to the genetic or phenotypic traits of the male. Though the role of future fitness in empirical results is often difficult to assess, female experience has been shown to influence reproductive investment. This result could indicate that experience informs the female’s assessment of current and future mating opportunities (i.e., expected future fitness). Here, we tested whether female experience and mate attractiveness affected offspring size and number in sheepshead swordtails. We manipulated mate attractiveness by feeding males different diets, as females have been shown to prefer well-fed males. We found that females exposed to well-fed males, and then mated to poorly fed males, produced the largest offspring. Clutch size increased more rapidly with female size for females with mates on a poor diet, independent of female experience. Our results suggest that swordtail females elevate their investment in offspring size and number when mated to poorly fed males. These results demonstrate that maternal investment can be influenced by female social environment and experience, with underappreciated consequences for offspring fitness.

While extensive empirical and theoretical work has focused on the evolution of costly cooperation (particularly in group-living species), less attention has been paid to more low-risk or immediately beneficial forms of cooperation. In some non-group-living darters, alloparental care (or allocare) by subordinates has been noted to result from by-product benefits as small territorial (subordinate) males adopt and provide care to the abandoned eggs of large territorial (dominant) males. In the tessellated darter (Etheostoma olmstedi), allocare also results from sneak fertilization. However, information on the rate of allocare by tessellated darters is contradictory: prior behavioral work suggested that it is very common, while a genetic examination showed males to primarily care for their own young. We found behavioral and genetic evidence of very high levels of allocare at our study location. The relative size of the assigned fathers of young to the alloparental male is consistent with the idea that initial allocare primarily results from sneak fertilization (“cuckoldry-based allocare”), but later allocare results from subordinate males caring at previously abandoned nests (“adoption-based allocare”). Larger males appeared to breed more frequently at different nests, but did not father more individual offspring than smaller males. Finally, low relatedness between abandoning and alloparenting males suggests that kin selection does not contribute to alloparental care. We discuss how variation in nest availability may explain the inconsistent findings of the rate of alloparental care in the tessellated darter, and how increased research in this and similar systems can expand our understanding of the evolution of cooperation.

Male-only care is the most frequent parental care behaviour in teleost fishes, but little is known about its evolutionary origins and patterns of diversity in species-rich lineages. Darters are a clade of North American freshwater fishes that contain both nonparental care species and species with male-only care. In darters, paternal care takes the form of egg-guarding and other egg-tending behaviours that are dependent on the female mode of egg deposition. Male care has been hypothesized to evolve independently in darters at least three times, and it has been thought to be irreversible. We investigated the diversification of egg-deposition behaviours and the evolution of complex male care using published descriptions of darter reproductive behaviours and a multilocus molecular phylogeny that included all 146 species for which reproductive behaviours are known. We find support for two origins of male-only care behaviour. One origin of paternal care occurred relatively early in the radiation of Etheostoma and is characteristic of a recently discovered clade, Goneaperca. The other origin of male-only care occurred much more recently in a derived clade of Nothonotus. Our analyses of character diversification demonstrate reversals from care to noncare and multiple transitions between egg-deposition behaviours that are not associated with parental care.

Life-history theory predicts that older females will increase reproductive effort through increased fecundity. Unless offspring survival is density dependent or female size constrains offspring size, theory does not predict variation in offspring size. However, empirical data suggest that females of differing age or condition produce offspring of different sizes. We used a dynamic state-variable model to determine when variable offspring sizes can be explained by an interaction between female age, female state and survival costs of reproduction. We found that when costs depend on fecundity, young females with surplus state increase offspring size and reduce number to minimize fitness penalties. When costs depend on total reproductive effort, only older females increase offspring size. Young females produce small offspring, because decreasing offspring size is less expensive than number, as fitness from offspring investment is nonlinear. Finally, allocation patterns are relatively stable when older females are better at acquiring food and are therefore in better condition. Our approach revealed an interaction between female state, age and survival costs, providing a novel explanation for observed variation in reproductive traits.

When individuals defend and care for young that are not their own (alloparental care), it raises the question of what benefits might lead to the evolution and persistence of such care. Here, we examine how male and female preferences affect the direct benefits of alloparental care. In the tessellated darter, alloparental care by some males often follows nest abandonment by others (Stiver KA, Wolff S, Alonzo SH, in preparation). We hypothesize that alloparental care may have evolved due to mating benefits: Alloparental care could be favored if females prefer to breed at nests that contain eggs. We found that, on average, males and females prefer nests with young eggs to those without eggs. Consequently, although young eggs increase the attractiveness of the nest, this positive effect is lost as the age of the eggs on the nest increases. We also found that alloparental care is costly in terms of future potential mating success as the amount of new eggs deposited in a nest decreases as nests become more filled. Therefore, alloparental males may initially increase their attractiveness to females by defending nests with another male’s eggs but still potentially gain fewer eggs relative to those received by males defending empty nests. Our findings shed light on the evolution of alloparental care in the tessellated darter, suggesting that female mating preferences may underlie this well-documented cooperative relationship between males. Key words: cooperation, female choice, mate-choice copying, predation dilution, sexual selection, tessellated darter. [Behav Ecol]

Although negative frequency-dependent fitness is argued to allow the stable coexistence of two alternative reproductive types (such as resource defenders and reproductive parasites), no existing theory has considered a third strategy where resource defenders invest differentially in defence against reproductive parasites. Here, we present the results of a three-strategy game, where reproductive parasites interact with two resource defenders: ‘Susceptibles’ defend more resources but lose more reproductive success to parasites. ‘Immunes’ lose less to parasites, but immunity carries a reproductive cost. We show that the inclusion of a third strategy dramatically changes the evolutionary dynamics, such that for a wide range of parameter values, our model predicts the continuous sequential invasion of the three strategies instead of stable coexistence. Our results therefore limit the generality of the prediction that frequency-dependent fitness necessarily allows alternative reproductive tactics to coexist at equilibrium and may also explain the observed dynamics of some multiple-strategy systems.

Theory predicts that the 'size advantage' (rate of increase in male and female fitness with age or size) determines the direction and the timing of sex change in sequential hermaphrodites. Whereas the size advantage is generated by the mating system and would be expected to vary within and between species, the shape or form of the size advantage has rarely been estimated directly. Here, we ask whether theoretical predictions about the timing of sex change hold under different types of size advantage. We model two biological scenarios representing different processes generating the size advantage and find that different types of size advantage can produce patterns that qualitatively differ from classic predictions. Our results demonstrate that a good understanding of sequentially hermaphroditic mating systems, and specifically, a direct assessment of the processes underlying the size advantage is crucial to reliably predict and explain within-species patterns of the timing of sex change.

Recent theory predicted that male advertisement will reliably signal investment in paternal care in species where offspring survival requires paternal care and males allocate resources between advertisement and care. However, the predicted relationship between care and advertisement depended on the marginal gains from investment in current reproductive traits. Life history theory suggests that these fitness gains are also subject to a trade-off between current and future reproduction. Here, we investigate whether male signalling remains a reliable indicator of parental care when males allocate resources between current advertisement, paternal care and survival to future reproduction. We find that advertisement is predicted to remain a reliable signal of male care but that advertisement may cease to reliably indicate male quality because low-quality males are predicted to invest in current reproduction, whereas higher-quality males are able to invest in both current reproduction and survival to future reproduction.

Theory suggests that males that are larger than their competitors may have increased mating success, due to both greater competitive ability and increased attractiveness to females. We examined how male mating success varies with male size in the tessellated darter Etheostoma olmstedi. Previous work has shown that large males tend to move around and breed in vacant breeding sites, and consequently provide less care for their eggs, while smaller individuals can be allopaternal, caring for the eggs of other males as well as for their own. We studied female egg deposition in a natural breeding population using artificial breeding sites and in the laboratory, where female choice of spawning site was restricted to two breeding sites tended by two males of different sizes. In both the field and the laboratory, nests tended by larger males were more likely to receive new eggs. Additionally, the mean size of males associated with a nest was positively correlated with both the maximum coverage of eggs at the nest and the number of times new eggs were deposited. We discuss how the increased mating success of larger males, despite their decreased parental care, may help explain allopaternal care in this species [Current Zoology 56 (1): 1–5 2010].

A survey of empirical studies relating mating and parental investment reveals as many unpredicted patterns as results supporting existing hypotheses. This leaves us with individual post hoc explanations of observed patterns rather than an ability to make strong a priori predictions. I argue here that our ability to explain and predict empirical patterns can be improved by considering how social interactions and coevolutionary dynamics affect male and female reproductive traits. Recent research suggests that these social and coevolutionary feedbacks can increase our understanding of empirical patterns, while suggesting new directions of research. I also describe a social and coevolutionary dynamics modelling approach that integrates ideas from reproductive cooperation and sexual conflict to increase understanding of mating and parental investment.

One of the common assumptions in the study of the evolution of parental care is that trade-offs exist between parental investment and other fitness-related traits. In general, this body of work follows the traditional definition that parental investment (in the current offspring) decreases that individual’s ability to invest in future reproduction (Trivers 1972). However, examination of the empirical evidence shows that assuming a trade-off between parental and mating effort is not always appropriate. This overemphasis on a trade-off between mating and parental effort has arisen in part because of an oversimplification of female reproductive strategies, a failure to consider interactions between the sexes, and a tendency to consider behaviours as unifunctional, thereby ignoring the more complex relationship between mating and parental effort in many species. Here, we first examine the empirical evidence for trade-offs between mating and parental effort in males and females to ask when trade-offs occur and what pattern they take. By highlighting a number of exemplar species, we then explore how the presence or absence of trade-offs relates to mate choice and sexual selection in both sexes. Finally, we highlight the importance of considering individual variation, which has been particularly overlooked in examinations of female investment, and how preferences in one sex may influence the existence and our interpretation of apparent trade-offs in the other sex.

Although theory generally predicts that males should reduce paternal care in response to cues that predict increased sperm competition and decreased paternity, empirical patterns are equivocal. Some studies have found the predicted decrease in male care with increased sperm competition, while even more studies report no effect of paternity or sperm competition on male care. Here, we report the first example, to our knowledge, of paternal care increasing with the risk and intensity of sperm competition, in the ocellated wrasse ( Symphodus ocellatus ). Theory also predicts that if paternal care varies and is important to female fitness, female choice among males and male indicators traits of expected paternal care should evolve. Despite a non-random distribution of mating success among nests, we found no evidence for female choice among parental males. Finally, we document the highest published levels of extra-pair paternity for a species with exclusive and obligate male care: genetic paternity analyses revealed cuckoldry at 100 per cent of nests and 28 per cent of all offspring were not sired by the male caring for them. While not predicted by any existing theory, these unexpected reproductive patterns become understandable if we consider how male and female mating and parental care interact simultaneously in this and probably many other species.

Existing theory predicts that male signalling can be an unreliable indicator of paternal care, but assumes that males with high levels of mating success can have high current reproductive success, without providing any parental care. As a result, this theory does not hold for the many species where offspring survival depends on male parental care. We modelled male allocation of resources between advertisement and care for species with male care where males vary in quality, and the effect of care and advertisement on male fitness is multiplicative rather than additive. Our model predicts that males will allocate proportionally more of their resources to whichever trait (advertisement or paternal care) is more fitness limiting. In contrast to previous theory, we find that male advertisement is always a reliable indicator of paternal care and male phenotypic quality (e.g. males with higher levels of advertisement never allocate less to care than males with lower levels of advertisement). Our model shows that the predicted pattern of male allocation and the reliability of male signalling depend very strongly on whether paternal care is assumed to be necessary for offspring survival and how male care affects offspring survival and male fitness.

Sex change is a relatively rare phenomenon among animals. While classic theory has been successful in assessing the adaptive significance of sex change and predicting within-species patterns, it does not explain why more animals are not sex changers. A possible explanation for the rarity of sex change is that costs such as decreased reproduction due to gonadal reconstruction favor separate sexes, or dioecy. These costs, however, have not been studied empirically or theoretically. Here, we investigate whether costs of changing sex can favor dioecy. Our analyses suggest that dioecy is favored only when costs of changing sex are large. Moreover, the fitness effect of costs and the strength of male size advantage are not static but change with the population composition, resulting in a dynamic evolutionary game between sex change and dioecy. We conclude that costs of changing sex alone are unlikely to explain the observed rarity of sex changers. Instead, assessing mating systems comparatively and quantitatively and identifying correlates selecting for and against sex change are necessary to understand why some species change sex while others do not.

Extensive research has focused on understanding the evolution of parental care, with fishes providing important model systems for understanding patterns of variation within and between species. Classic theory predicts that individuals will care for offspring when the fitness benefits through increased offspring survival and growth outweigh the cost to the parents through decreased future reproductive opportunities. Yet, a puzzling observation not explained by this basic theory is the fact that in some species individuals defend and provision unrelated offspring and thus exhibit alloparental care. The tessellated darter, Etheostoma olmstedi, represents one of the first known examples of allopaternal care in fishes. In this species, males often clean and guard eggs fertilized but deserted by other males. Allopaternal care has been argued to occur in the tessellated darter because of competition for a limited number of mating sites where less dominant males accept territories with eggs when other breeding sites are not available. Here, we test this hypothesis using male territory choice experiments. When allowed to choose between two otherwise identical territories either containing eggs fertilized by another male or with no eggs, males spent significantly more time at territories with eggs. This demonstrates that competition for mating territories is not the primary factor explaining the existence of allopaternal care in the tessellated darter. Instead, males of this species may exhibit allopaternal care to dilute predator pressure on their own eggs or because females prefer to mate with males whose territories contain eggs.