Does losing reduce the tendency to engage with rivals to reach mates? An experimental test.

Male-male contests for access to females or breeding resources are critical in determining male reproductive success. Larger males and those with more effective weaponry are more likely to win fights. However, even after controlling for such predictors of fighting ability, studies have reported a winner-loser effect: previous winners are more likely to win subsequent contests, while losers often suffer repeated defeats. While the effect of winning-losing is well-documented for the outcome of future fights, its effect on other behaviors (e.g. mating) remains poorly investigated. Here, we test whether a winning versus losing experience influenced subsequent behaviors of male mosquitofish (Gambusia holbrooki) toward rivals and potential mates. We housed focal males with either a smaller or larger opponent for 24 h to manipulate their fighting experience to become winners or losers, respectively. The focal males then underwent tests that required them to enter and swim through a narrow corridor to reach females, bypassing a cylinder that contained either a larger rival male (competitive scenario), a juvenile or was empty (non-competitive scenarios). The tests were repeated after 1 wk. Winners were more likely to leave the start area and to reach the females, but only when a larger rival was presented, indicating higher levels of risk-taking behavior in aggressive interactions. This winner-loser effect persisted for at least 1 wk. We suggest that male mosquitofish adjust their assessment of their own and/or their rival's fighting ability following contests in ways whose detection by researchers depends on the social context.

Does the potential strength of sexual selection differ between mating systems with and without defensive behaviours? A meta-analysis.

The Darwin-Bateman paradigm predicts that females enhance their fitness by being choosy and mating with high-quality males, while males should compete to mate with as many females as possible. In many species, males enhance their fitness by defending females and/or resources used by females. That is, males directly defend access to mating opportunities. However, paternity analyses have repeatedly shown that females in most species mate polyandrously, which contradicts traditional expectations that male defensive behaviours lead to monandry. Here, in an extensive meta-analysis, encompassing 109 species and 1026 effect sizes from across the animal kingdom, we tested if the occurrence of defensive behaviours modulates sexual selection on females and males. If so, we can illuminate the extent to which males really succeed in defending access to mating and fertilisation opportunities. We used four different indices of the opportunity for sexual selection that comprise pre-mating and/or post-mating episodes of selection. We found, for both sexes, that the occurrence of defensive behaviours does not modulate the potential strength of sexual selection. This implies that male defensive behaviours do not predict the true intensity of sexual selection. While the most extreme levels of sexual selection on males are in species with male defensive behaviours, which indicates that males do sometimes succeed in restricting females' re-mating ability (e.g. elephant seals, Mirounga leonina), estimates of the opportunity for sexual selection vary greatly across species, regardless of whether or not defensive behaviours occur. Indeed, widespread polyandry shows that females are usually not restricted by male defensive behaviours. In addition, our results indicate that post-mating episodes of selection, such as cryptic female choice and sperm competition, might be important factors modulating the opportunity for sexual selection. We discuss: (i) why male defensive behaviours fail to lower the opportunity for sexual selection among females or fail to elevate it for males; (ii) how post-mating events might influence sexual selection; and (iii) the role of females as active participants in sexual selection. We also highlight that inadequate data reporting in the literature prevented us from extracting effect sizes from many studies that had presumably collected the relevant data.

Fitness as the organismal performance measure guiding adaptive evolution.

A long-standing problem in evolutionary theory is to clarify in what sense (if any) natural selection cumulatively improves the design of organisms. Various concepts, such as fitness and inclusive fitness, have been proposed to resolve this problem. In addition, there have been attempts to replace the original problem with more tractable questions such as whether a given gene or trait is favoured by selection. Here we ask what theoretical properties the concept fitness should possess to encapsulate the improvement criterion required to talk meaningfully about adaptive evolution. We argue that natural selection tends to shape phenotypes based on the causal properties of individuals, and that this tendency is therefore best captured by a fitness concept that focusses on these properties. We highlight a fitness concept which meets this role under broad conditions, but requires adjustments in our conceptual understanding of adaptive evolution. These adjustments combine elements of Dawkinsian gene selectionism and Egbert Leigh's "parliament of genes".

Sexual dimorphism in subterranean amphipod crustaceans covaries with subterranean habitat type.

Sexual dimorphism can evolve in response to sex-specific selection pressures that vary across habitats. We studied sexual differences in subterranean amphipods Niphargus living in shallow subterranean habitats (close to the surface), cave streams (intermediate), and cave lakes (deepest and most isolated). These three habitats differ because at greater depths there is lower food availability, reduced predation, and weaker seasonality. Additionally, species near the surface have a near-even adult sex ratio (ASR), whereas species from cave lakes have a female-biased ASR. We hypothesized (a) a decrease in sexual dimorphism from shallow subterranean habitats to cave lake species because of weaker sexual selection derived from changes in the ASR and (b) an increase in female body size in cave lakes because of stronger fecundity selection on account of oligotrophy, reduced predation, and weaker seasonality. We measured body size and two sexually dimorphic abdominal appendages for all 31 species and several behaviours related to male competition (activity, risk-taking, exploration) for 12 species. Species with an equal ASR that live close to the surface exhibited sexual dimorphism in all three morphological traits, but not in behaviour. The body size of females increased from the surface to cave lakes, but no such trend was observed in males. In cave lake species, males and females differed neither morphologically nor behaviourally. Our results are consistent with the possibility that sexual and fecundity selection covary across the three habitats, which indirectly and directly, respectively, shape the degree of sexual dimorphism in Niphargus species.

Effects of past mating behavior versus past ejaculation on male mate choice and male attractiveness.

Past reproductive effort allows males to assess their ability to acquire mates, but it also consumes resources that can reduce their future competitive ability. Few studies have examined how a male's reproductive history affects his subsequent mate choice, and, to date, no study has determined the relative contribution of past mating behavior and past ejaculate production because these two forms of investment are naturally highly correlated. Here, we disentangled the relative effects of past mating behavior and past ejaculate production in mosquitofish (Gambusia holbrooki) by experimentally preventing some males from ejaculating when trying to mate. We assessed the effect of mating behavior on mate choice by comparing males that had previously been with or without access to females and male rivals for 8 and 16 weeks and assessed the effect of ejaculation on mate choice by comparing males that either could or could not ejaculate when they had access to females for 16 weeks. Reproductive treatment did not affect male attractiveness, but it did affect male mate choice. Somewhat surprisingly, in five of the six treatment-by-age at testing combinations, males preferred a female in the vicinity of a male rival over a solitary female. This preference was marginally stronger for males that had previously engaged in mating behavior but were unaffected by past ejaculate production. We discuss the potential benefits to males of associating with another male when seeking mates. This is the first study to quantify the relative influence of pre- and post-copulatory reproductive investment on male mate choice.

Mitochondrial function and sexual selection: can physiology resolve the 'lek paradox'?

Across many taxa, males use elaborate ornaments or complex displays to attract potential mates. Such sexually selected traits are thought to signal important aspects of male 'quality'. Female mating preferences based on sexual traits are thought to have evolved because choosy females gain direct benefits that enhance their lifetime reproductive success (e.g. greater access to food) and/or indirect benefits because high-quality males contribute genes that increase offspring fitness. However, it is difficult to explain the persistence of female preferences when males only provide genetic benefits, because female preferences should erode the heritable genetic variation in fitness that sexually selected traits signal. This 'paradox of the lek' has puzzled evolutionary biologists for decades, and inspired many hypotheses to explain how heritable variation in sexually selected traits is maintained. Here, we discuss how factors that affect mitochondrial function can maintain variation in sexually selected traits despite strong female preferences. We discuss how mitochondrial function can influence the expression of sexually selected traits, and we describe empirical studies that link the expression of sexually selected traits to mitochondrial function. We explain how mothers can affect mitochondrial function in their offspring by (a) influencing their developmental environment through maternal effects and (b) choosing a mate to increase the compatibility of mitochondrial and nuclear genes (i.e. the 'mitonuclear compatibility model of sexual selection'). Finally, we discuss how incorporating mitochondrial function into models of sexual selection might help to resolve the paradox of the lek, and we suggest avenues for future research.

Publication bias impacts on effect size, statistical power, and magnitude (Type M) and sign (Type S) errors in ecology and evolutionary biology.

Collaborative efforts to directly replicate empirical studies in the medical and social sciences have revealed alarmingly low rates of replicability, a phenomenon dubbed the 'replication crisis'. Poor replicability has spurred cultural changes targeted at improving reliability in these disciplines. Given the absence of equivalent replication projects in ecology and evolutionary biology, two inter-related indicators offer the opportunity to retrospectively assess replicability: publication bias and statistical power. This registered report assesses the prevalence and severity of small-study (i.e., smaller studies reporting larger effect sizes) and decline effects (i.e., effect sizes decreasing over time) across ecology and evolutionary biology using 87 meta-analyses comprising 4,250 primary studies and 17,638 effect sizes. Further, we estimate how publication bias might distort the estimation of effect sizes, statistical power, and errors in magnitude (Type M or exaggeration ratio) and sign (Type S). We show strong evidence for the pervasiveness of both small-study and decline effects in ecology and evolution. There was widespread prevalence of publication bias that resulted in meta-analytic means being over-estimated by (at least) 0.12 standard deviations. The prevalence of publication bias distorted confidence in meta-analytic results, with 66% of initially statistically significant meta-analytic means becoming non-significant after correcting for publication bias. Ecological and evolutionary studies consistently had low statistical power (15%) with a 4-fold exaggeration of effects on average (Type M error rates = 4.4). Notably, publication bias reduced power from 23% to 15% and increased type M error rates from 2.7 to 4.4 because it creates a non-random sample of effect size evidence. The sign errors of effect sizes (Type S error) increased from 5% to 8% because of publication bias. Our research provides clear evidence that many published ecological and evolutionary findings are inflated. Our results highlight the importance of designing high-power empirical studies (e.g., via collaborative team science), promoting and encouraging replication studies, testing and correcting for publication bias in meta-analyses, and adopting open and transparent research practices, such as (pre)registration, data- and code-sharing, and transparent reporting.

The Effect of Brief or Prolonged Bouts of Winning or Losing Male-Male Contests on Plasticity in Sexually Selected Traits.

AbstractFight outcomes often affect male fitness by determining their access to mates. Thus, "winner-loser" effects, where winners often win their next contest while losers tend to lose, can influence how males allocate resources toward pre- and postcopulatory traits. We experimentally manipulated the winning/losing experiences of pairs of size-matched male Gambusia holbrooki for 1 day, 1 week, or 3 weeks to test whether prior winning/losing experiences differentially affect the plasticity of male investment into either mating effort (precopulatory) or ejaculates (postcopulatory). When winner/loser pairs directly competed for a female, winners had better precopulatory outcomes than losers for three of the four traits we measured: mating attempts, successful attempts, and time spent with the female (but not aggression). However, winners and losers did not differ in either total sperm counts or sperm velocity. Interestingly, absolute male size, an important predictor of fighting success, mediated winner-loser effects on how long males then spent near a female. Compared with losers, smaller winners spent more time with the female than did larger winners, suggesting that how males respond to prior social experiences is size dependent. We discuss the general importance of controlling for inherent male condition when comparing male investment into condition-dependent traits.

Is more always better when it comes to mating?

Fitness usually increases when a male mates with more females, but is the same true for females? A new meta-analysis in PLOS Biology shows that females, like males, tend to have a positive relationship between the number of mates and their reproductive output. But why?

Sex roles and sex ratios in animals.

In species with separate sexes, females and males often differ in their morphology, physiology and behaviour. Such sex-specific traits are functionally linked to variation in reproductive competition, mate choice and parental care, which have all been linked to sex roles. At the 150th anniversary of Darwin's theory on sexual selection, the question of why patterns of sex roles vary within and across species remains a key topic in behavioural and evolutionary ecology. New theoretical, experimental and comparative evidence suggests that variation in the adult sex ratio (ASR) is a key driver of variation in sex roles. Here, we first define and discuss the historical emergence of the sex role concept, including recent criticisms and rebuttals. Second, we review the various sex ratios with a focus on ASR, and explore its theoretical links to sex roles. Third, we explore the causes, and especially the consequences, of biased ASRs, focusing on the results of correlational and experimental studies of the effect of ASR variation on mate choice, sexual conflict, parental care and mating systems, social behaviour, hormone physiology and fitness. We present evidence that animals in diverse societies are sensitive to variation in local ASR, even on short timescales, and propose explanations for conflicting results. We conclude with an overview of open questions in this field integrating demography, life history and behaviour.

Protected areas and the future of insect conservation.

Anthropogenic pressures are driving insect declines across the world. Although protected areas (PAs) play a prominent role in safeguarding many vertebrate species from human-induced threats, insects are not widely considered when designing PA systems or building strategies for PA management. We review the effectiveness of PAs for insect conservation and find substantial taxonomic and geographic gaps in knowledge. Most research focuses on the representation of species, and few studies assess threats to insects or the role that effective PA management can play in insect conservation. We propose a four-step research agenda to help ensure that insects are central in efforts to expand the global PA network under the Post-2020 Global Biodiversity Framework.

Adult sex ratios: causes of variation and implications for animal and human societies.

Converging lines of inquiry from across the social and biological sciences target the adult sex ratio (ASR; the proportion of males in the adult population) as a fundamental population-level determinant of behavior. The ASR, which indicates the relative number of potential mates to competitors in a population, frames the selective arena for competition, mate choice, and social interactions. Here we review a growing literature, focusing on methodological developments that sharpen knowledge of the demographic variables underlying ASR variation, experiments that enhance understanding of the consequences of ASR imbalance across societies, and phylogenetic analyses that provide novel insights into social evolution. We additionally highlight areas where research advances are expected to make accelerating contributions across the social sciences, evolutionary biology, and biodiversity conservation.

In the shadows: wildlife behaviour in tree plantations.

Destruction of natural habitats for tree plantations is a major threat to wildlife. These novel environments elicit behavioural changes that can either be detrimental or beneficial to survival and reproduction, with population - and community - level consequences. However, compared with well-documented changes following other forms of habitat modification, we know little about wildlife behavioural responses to tree plantations, and even less about their associated fitness costs. Here, we highlight critical knowledge gaps in understanding the ecological and evolutionary consequences of behavioural shifts caused by tree plantations and discuss how wildlife responses to plantations could be critical in determining which species persist in these highly modified environments.

Separating the effects of paternal age and mating history: Evidence for sex-specific paternal effect in eastern mosquitofish.

Paternal age and past mating effort by males are often confounded, which can affect our understanding of a father's age effects. To our knowledge, only a few studies have standardized mating history when testing for effects of paternal age, and none has simultaneously disentangled how paternal age and mating history might jointly influence offspring traits. Here, we experimentally manipulated male mating history to tease apart its effects from those of paternal age on female fertility and offspring traits in the eastern mosquitofish (Gambusia holbrooki). Male age did not affect female fertility. However, males with greater past mating effort produced significantly larger broods. Paternal age and mating history interacted to affect sons' body size: sons sired by old-virgin males were larger than those sired by old-mated males, but this was not the case for younger fathers. Intriguingly, however, sons sired by old-virgin males tended to produce fewer sperms than those sired by old-mated males, indicating a potential trade-off in beneficial paternal effects. Finally, neither paternal age nor mating history affected daughter's fitness. Our results highlight that variation in offspring traits attributed to paternal age effect could partly arise due to a father's mating history, and not simply to his chronological age.

Male alternative reproductive tactics and sperm competition: a meta-analysis.

In many animal species, males may exhibit one of several discrete, alternative ways of obtaining fertilisations, known as alternative reproductive tactics (ARTs). Males exhibiting ARTs typically differ in the extent to which they invest in traits that improve their mating success, or the extent to which they face sperm competition. This has led to the widespread prediction that males exhibiting ARTs associated with a high sperm competition risk, or lower investment into traits that improve their competitiveness before mating, should invest more heavily into traits that improve their competitiveness after mating, such as large ejaculates and high-quality sperm. However, despite many studies investigating this question since the 1990s, evidence for differences in sperm and ejaculate investment between male ARTs is mixed, and there has been no quantitative summary of this field. Following a systematic review of the literature, we performed a meta-analysis examining how testes size, sperm number and sperm traits differ between males exhibiting ARTs that face either a high or low sperm competition risk, or high or low investment in traits that increase mating success. We obtained data from 92 studies and 67 species from across the animal kingdom. Our analyses showed that male fish exhibiting ARTs facing a high sperm competition risk had significantly larger testes (after controlling for body size) than those exhibiting tactics facing a low sperm competition risk. However, this effect appears to be due to the inappropriate use of the gonadosomatic index as a body-size corrected measure of testes investment, which overestimates the difference in testes investment between male tactics in most cases. We found no significant difference in sperm number between males exhibiting different ARTs, regardless of whether sperm were measured from the male sperm stores or following ejaculation. We also found no significant difference in sperm traits between males exhibiting different ARTs, with the exception of sperm adenosine triphosphate (ATP) content in fish. Finally, the difference in post-mating investment between male ARTs was not influenced by the extent to which tactics were flexible, or by the frequency of sneakers in the population. Overall, our results suggest that, despite clear theoretical predictions, there is little evidence that male ARTs differ substantially in investment into sperm and ejaculates across species. The incongruence between theoretical and empirical results could be explained if (i) theoretical models fail to account for differences in overall resource levels between males exhibiting different ARTs or fundamental trade-offs between investment into different ejaculate and sperm traits, and (ii) studies often use sperm or ejaculate traits that do not reflect overall post-mating investment accurately or affect fertilisation success.

A meta-analysis of sex differences in animal personality: no evidence for the greater male variability hypothesis.

The notion that men are more variable than women has become embedded into scientific thinking. For mental traits like personality, greater male variability has been partly attributed to biology, underpinned by claims that there is generally greater variation among males than females in non-human animals due to stronger sexual selection on males. However, evidence for greater male variability is limited to morphological traits, and there is little information regarding sex differences in personality-like behaviours for non-human animals. Here, we meta-analysed sex differences in means and variances for over 2100 effects (204 studies) from 220 species (covering five broad taxonomic groups) across five personality traits: boldness, aggression, activity, sociality and exploration. We also tested if sexual size dimorphism, a proxy for sex-specific sexual selection, explains variation in the magnitude of sex differences in personality. We found no significant differences in personality between the sexes. In addition, sexual size dimorphism did not explain variation in the magnitude of the observed sex differences in the mean or variance in personality for any taxonomic group. In sum, we find no evidence for widespread sex differences in variability in non-human animal personality.

Disentangling the effects of male age and mating history: Contrasting effects of mating history on precopulatory mating behavior and paternity success.

Many studies ask whether young or older males are better at acquiring mates. Even so, how age affects reproductive success is still poorly understood because male age and mating history are confounded in most studies: older males usually have more mating experience. To what extent does mating history rather than age explain variation in male mating success? And how do mating history and male age determine paternity when there is also postcopulatory sexual selection? Here, we experimentally manipulated the mating history of old and young males in the eastern mosquitofish (Gambusia holbrooki). We then recorded male mating behavior and share of paternity (1259 offspring from 232 potential sires) when they competed for mates and fertilizations. Old males, and males with no mating experience, spent significantly more time approaching females, and attempting to mate, than did young males and those with greater mating experience. Male age and mating history interacted to affect paternity: old males benefited from having previous mating experience, but young males did not. Our results highlight that the age-related changes in male reproductive traits and in paternity that have been described in many taxa may be partly attributable to male mating history and not simply to age itself.

Quantifying the costs of pre- and postcopulatory traits for males: Evidence that costs of ejaculation are minor relative to mating effort.

Although it is widely stated that both mating behavior and sperm traits are energetically costly for males, we currently lack empirical estimates of the relative costs to males of pre- versus postcopulatory investments. Such estimates require the experimental separation of the act of mating from that of ejaculation, which is a nontrivial logistical challenge. Here, we overcome this challenge using a novel morphological manipulation (gonopodium tip ablation) in the eastern mosquitofish (Gambusia holbrooki) to tease apart investment in mating effort from that in sperm replenishment following ejaculation. We quantified the relative cumulative costs of investing in mating effort and ejaculation by comparing somatic traits and reproductive performance among three types of males: ablated males that could attempt to mate but not ejaculate; unablated males that could both mate and ejaculate; and control males that had no access to females. We show that, after eight weeks, mating investment significantly reduces both body growth and immunocompetence and results in a significant decline in mating effort. In contrast, cumulative investment into sperm replenishment following ejaculation has few detectable effects that are only apparent in smaller males. These minor costs occur despite the fact that G. holbrooki has very high levels of sperm competition and multiple mating by both sexes, which is usually associated with elevated levels of sperm production. Crucially, our study is the first, to our knowledge, to experimentally compare the relative costs of pre- and postcopulatory investment on components of male fitness in a vertebrate.