The evolution of mating preferences for genetic attractiveness and quality in the presence of sensory bias.

The aesthetic preferences of potential mates have driven the evolution of a baffling diversity of elaborate ornaments. Which fitness benefit-if any-choosers gain from expressing such preferences is controversial, however. Here, we simulate the evolution of preferences for multiple ornament types (e.g., "Fisherian," "handicap," and "indicator" ornaments) that differ in their associations with genes for attractiveness and other components of fitness. We model the costs of preference expression in a biologically plausible way, which decouples costly mate search from cost-free preferences. Ornaments of all types evolved in our model, but their occurrence was far from random. Females typically preferred ornaments that carried information about a male's quality, defined here as his ability to acquire and metabolize resources. Highly salient ornaments, which key into preexisting perceptual biases, were also more likely to evolve. When males expressed quality-dependent ornaments, females invested readily in costly mate search to locate preferred males. In contrast, the genetic benefits associated with purely arbitrary ornaments were insufficient to sustain highly costly mate search. Arbitrary ornaments could nonetheless "piggyback" on mate-search effort favored by other, quality-dependent ornaments. We further show that the potential to produce attractive male offspring ("sexy sons") can be as important as producing offspring of high general quality ("good genes") in shaping female preferences, even when preferred ornaments are quality dependent. Our model highlights the importance of mate-search effort as a driver of aesthetic coevolution.

Long-term persistence of exaggerated ornaments under Fisherian runaway despite costly mate search.

Exaggerated ornaments often evolve due to the mating preferences of the opposite sex. Genetic correlations between preferences and ornaments can lead both traits to elaborate dramatically in tandem, in a process known as 'Fisherian runaway'. However, in most previous models of Fisherian runaway, elaborate ornaments are not expected to persist when preferences are consistently costly to the choosing sex. In contrast, we show here that exaggerated male ornaments can be maintained long term even when females must pay a cost to choose their mates. Preferences per se are not costly in our model, but females can only act on their preferences by investing resources in mate search. We predict that mate search effort should decrease with the cost of sampling additional mates and increase with the number of possible ornaments that females can choose from. The potential for multiple exaggerated ornaments to coexist depends on subtleties of their cost structure: strict trade-offs (additive costs) favour sequential ornament evolution, whereas looser trade-offs (multiplicative costs) allow for coexistence. Lastly, we show that pleiotropy affecting both ornaments and preferences makes it difficult for Fisherian runaway to initiate, increasing the evolutionary time until ornamentation. Our model highlights the important but neglected role of mate search effort in sexual selection.

Inclusive fitness benefits mitigate costs of cuckoldry to socially paired males.

BACKGROUND: In socially monogamous species, reproduction is not always confined to paired males and females. Extra-pair males commonly also reproduce with paired females, which is traditionally thought to be costly to the females' social partners. However, we suggest that when the relatedness between reproducing individuals is considered, cuckolded males can suffer lower fitness losses than otherwise expected, especially when the rate of cuckoldry is high. We combine theoretical modeling with a detailed genetic study on a socially monogamous wild fish, Variabilichromis moorii, which displays biparental care despite exceptionally high rates of extra-pair paternity. RESULTS: We measured the relatedness between all parties involved in V. moorii spawning events (i.e. between males and females in social pairs, females and their extra-pair partners, and paired males and their cuckolders), and we reveal that males are on average more related to their cuckolders than expected by chance. Queller-Goodnight estimates of relatedness between males and their cuckolders are on average r = 0.038 but can range up to r = 0.64. This also increases the relatedness between males and the extra-pair offspring under their care. These intriguing results are consistent with the predictions of our mathematical model, which shows that elevated relatedness between paired males and their cuckolders can be adaptive for both parties when competition for fertilizations is strong. CONCLUSIONS: Our results show how cuckoldry by relatives can offset males' direct fitness losses with inclusive fitness gains, which can be substantial in systems where males face almost certain paternity losses.

Nest defense in the face of cuckoldry: evolutionary rather than facultative adaptation to chronic paternity loss.

BACKGROUND: Raising unrelated offspring is typically wasteful of parental resources and so individuals are expected to reduce or maintain low levels of parental effort when their parentage is low. This can involve facultative, flexible adjustments of parental care to cues of lost parentage in the current brood, stabilizing selection for a low level of paternal investment, or an evolutionary reduction in parental investment in response to chronically low parentage. RESULTS: We studied parental care in Variabilichromis moorii, a socially monogamous, biparental cichlid fish, whose mating system is characterized by frequent cuckoldry and whose primary form of parental care is offspring defense. We combine field observations with genetic parentage analyses to show that while both parents defend their nest against intruding con- and hetero-specifics, males and females may do so for different reasons. Males in the study group (30 breeding pairs) sired 0-100% (median 83%) of the fry in their nests. Males defended less against immediate threats to the offspring, and more against threats to their territories, which are essential for the males' future reproductive success. Males also showed no clear relationship between their share of defense and their paternity of the brood. Females, on the other hand, were related to nearly all the offspring under their care, and defended almost equally against all types of threats. CONCLUSION: Overall, males contributed less to defense than females and we suggest that this asymmetry is the result of an evolutionary response by males to chronically high paternity loss in this species. Although most males in the current study group achieved high parentage in their nests, the average paternity in V. moorii, sampled across multiple seasons, is only about 55%. We highlight the importance and complexity of studying nest defense as a form of parental care in systems where defense may serve not only to protect current offspring, but also to ensure future reproductive success by maintaining a territory.

Sex roles and the evolution of parental care specialization.

Males and females are defined by the relative size of their gametes (anisogamy), but secondary sexual dimorphism in fertilization, parental investment and mating competition is widespread and often remarkably stable over evolutionary timescales. Recent theory has clarified the causal connections between anisogamy and the most prevalent differences between the sexes, but deviations from these patterns remain poorly understood. Here, we study how sex differences in parental investment and mating competition coevolve with parental care specialization. Parental investment often consists of two or more distinct activities (e.g. provisioning and defence) and parents may care more efficiently by specializing in a subset of these activities. Our model predicts that efficient care specialization broadens the conditions under which biparental investment can evolve in lineages that historically had uniparental care. Major transitions in sex roles (e.g. from female-biased care with strong male mating competition to male-biased care with strong female competition) can arise following ecologically induced changes in the costs or benefits of different care types, or in the sex ratio at maturation. Our model provides a clear evolutionary mechanism for sex-role transitions, but also predicts that such transitions should be rare. It consequently contributes towards explaining widespread phylogenetic inertia in parenting and mating systems.

A rigorous comparison of sexual selection indexes via simulations of diverse mating systems.

Sexual selection is a cornerstone of evolutionary theory, but measuring it has proved surprisingly difficult and controversial. Various proxy measures--e.g., the Bateman gradient and the opportunity for sexual selection--are widely used in empirical studies. However, we do not know how reliably these measures predict the strength of sexual selection across natural systems, and most perform poorly in theoretical worst-case scenarios. Here we provide a rigorous comparison of eight commonly used indexes of sexual selection. We simulated 500 biologically plausible mating systems, based on the templates of five well-studied species that cover a diverse range of reproductive life histories. We compared putative indexes to the actual strength of premating sexual selection, measured as the strength of selection on a simulated "mating trait." This method sidesteps a key weakness of empirical studies, which lack an appropriate yardstick against which proxy measures can be assessed. Our model predicts that, far from being useless, the best proxy measures reliably track the strength of sexual selection across biologically realistic scenarios. The maximum intensity of precopulatory sexual selection s'max (the Jones index) outperformed all other indexes and was highly correlated with the strength of sexual selection. In contrast, the Bateman gradient and the opportunity for sexual selection were poor predictors of sexual selection, despite their continuing popularity.

Brood-tending males in a biparental fish suffer high paternity losses but rarely cuckold.

Extra-pair paternity within socially monogamous mating systems is well studied in birds and mammals but rather neglected in other animal taxa. In fishes, social monogamy has evolved several times but few studies have investigated the extent to which pair-bonded male fish lose fertilizations to cuckolders and gain extra-pair fertilizations themselves. We address this gap and present genetic paternity data collected from a wild population of Variabilichromis moorii, a socially monogamous African cichlid with biparental care of offspring. We show that brood-tending, pair-bonded males suffer exceptionally high paternity losses, siring only 63% of the offspring produced by their female partners on average. The number of cuckolders per brood ranged up to nine and yet, surprisingly, brood-tending males in the population were rarely the culprits. Brood-tending males sired very few extra-pair offspring, despite breeding in close proximity to one another. While unpaired males were largely responsible for the cuckoldry, pair-bonded males still enjoyed higher fertilization success than individual unpaired males. We discuss these results in the context of ecological and phenotypic constraints on cuckoldry and the fitness payoffs of alternative male tactics. Our study provides new insights into how pair-bonded males handle the trade-off between securing within-pair and extra-pair reproduction.

Finding the one: optimal choosiness under sequential mate choice.

When mates are encountered sequentially, each encounter involves a decision whether to reject the current suitor and risk not finding a better mate, or to accept them despite their flaws. I provide a flexible framework for modelling optimal choosiness when mate encounters occur unpredictably in time. The model allows for temporal variation in the fitness benefits of mating, including seasonal breeding conditions, accrual of mate search costs, survival of the choosing individual or senescence of gametes. The basic optimality framework can be applied iteratively to obtain mate choice equilibria in dynamically evolving populations. My model predicts that individuals should be choosier when the average rate of mate encounters is high, but that choosiness should decline over time as the likelihood of future mate encounters decreases. When mate encounters are uncertain, there is a trade-off between reproductive timing and mate choice (the 'when' and the 'who'). Mate choice may be selected against when reproductive timing is highly important (e.g. when breeding conditions show a narrow peak in time). This can even lead to step-shaped mate choice functions, where individuals abruptly switch from rejecting to accepting all suitors as peak breeding conditions approach. The model contributes to our understanding of why individuals may not express mate preferences, even when there is substantial variation in mate quality.

Sexual selection on male body size, genital length and heterozygosity: Consistency across habitats and social settings.

Spatial and temporal variation in environmental factors and the social setting can help to maintain genetic variation in sexually selected traits if it affects the strength of directional selection. A key social parameter which affects the intensity of, and sometimes predicts the response to, mating competition is the operational sex ratio (OSR; ratio of receptive males to females). How the OSR affects selection for specific male traits is poorly understood. It is also unclear how sexual selection is affected by interactions between the OSR and environmental factors, such as habitat complexity, that alter key male-female interactions such as mate encounter rates. Here, we experimentally manipulated the OSR and habitat complexity and quantified sexual selection on male mosquitofish (Gambusia holbrooki) by directly measuring male reproductive success (i.e. paternity). We show that despite a more equitable sharing of paternity (i.e. higher levels of multiple paternity) under a male-biased OSR, selection on focal male traits was unaffected by the OSR or habitat complexity. Instead, sexual selection consistently, and significantly, favoured smaller bodied males, males with higher genome wide heterozygosity (based on >3,000 SNP markers) and males with a relatively long gonopodium (intromittent organ). Our results show that sexual selection on male body size, relative genital size and heterozygosity in this system is consistent across environments that vary in ecological parameters that are expected to influence mate encounter rates.

Local gamete competition explains sex allocation and fertilization strategies in the sea.

Within and across taxa, there is much variation in the mode of fertilization, that is, whether eggs and/or sperm are released or kept inside or on the surface of the parent's body. Although the evolutionary consequences of fertilization mode are far-reaching, transitions in the fertilization mode itself have largely escaped theoretical attention. Here we develop the first evolutionary model of egg retention and release, which also considers transitions between hermaphroditism and dioecy as well as egg size evolution. We provide a unifying explanation for reported associations between small body size, hermaphroditism, and egg retention in marine invertebrates that have puzzled researchers for more than 3 decades. Our model, by including sperm limitation, shows that all these patterns can arise as an evolutionary response to local competition between eggs for fertilization. This can provide a general explanation for three empirical patterns: sperm casters tend to be smaller than related broadcast spawners, hermaphroditism is disproportionately common in sperm casters, and offspring of sperm casters are larger. Local gamete competition also explains a universal sexual asymmetry: females of some species retain their gametes while males release theirs, but the opposite ("egg casting") lacks evolutionary stability and is apparently not found in nature.

Is biased mutation sufficient to save runaway sexual selection?

In the 1980s, groundbreaking theoretical studies showed that orna- ments displayed during courtship can coevolve with preferences for such ornaments, leading to extreme exaggeration of both traits. Later mod- els cast doubt on such 'runaway' sexual selection, showing that even a small cost of preferences can prevent exaggerated ornaments from per- sisting long-term. It was subsequently shown that if mutations acting on the ornament are biased - tending to produce smaller rather than larger ornaments - then exaggeration can persist even in the presence of pref- erence costs, seemingly vindicating the original models. Here, we unpack an implicit assumption of these 'biased mutation' models: Mutations are assumed to lead, on average, to both smaller and less costly ornaments. Biased mutation consequently generates both a fitness cost (due to re- duced mating success) and a fitness benefit (due to increased survival). We lift this assumption by separating an individual's investment in an or- nament from their efficiency in converting such investment into ornament size. We assume that biased mutation acts only on efficiency, but not on investment, and discuss the plausibility of this alternative assumption. Our model predicts that exaggerated ornaments and preferences can per- sist stably once they arise, but that strong initial preferences are needed to kick-start the runaway process. Consequently, biased mutation alone may not always be sufficient to save runaway sexual selection.

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 favored 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 focuses on these properties. We highlight a fitness concept that 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."

Hermaphroditic origins of anisogamy.

Anisogamy-the size dimorphism of gametes-is the defining difference between the male and female sexual strategies. Game-theoretic thinking led to the first convincing explanation for the evolutionary origins of anisogamy in the 1970s. Since then, formal game-theoretic models have continued to refine our understanding of when and why anisogamy should evolve. Such models typically presume that the earliest anisogamous organisms had separate sexes. However, in most taxa, there is no empirical evidence to support this assumption. Here, we present a model of the coevolution of gamete size and sex allocation, which allows for anisogamy to emerge alongside either hermaphroditism or separate sexes. We show that hermaphroditic anisogamy can evolve directly from isogamous ancestors when the average size of spawning groups is small and fertilization is relatively efficient. Sex allocation under hermaphroditism becomes increasingly female-biased as group size decreases and the degree of anisogamy increases. When spawning groups are very small, our model also predicts the existence of complex isogamous organisms in which individuals allocate resources equally to two large gamete types. We discuss common, but potentially unwarranted, assumptions in the literature that could be relaxed in future models. This article is part of the theme issue 'Half a century of evolutionary games: a synthesis of theory, application and future directions'.

Seasonal variation in cuckoldry rates in the socially monogamous cichlid fish Variabilichromis moorii.

Mating patterns in animal populations can respond to environmental conditions and consequently vary across time. To examine this variation in nature, studies must include temporal replicates from the same population. Here, we report temporal variation in genetic parentage in the socially monogamous cichlid Variabilichromis moorii from Lake Tanganyika, using samples of broods and their brood-tending parents that were collected across five field trips from the same study population. The sampled broods were either spawned during the dry season (three field trips) or during the rainy season (two trips). In all seasons, we detected substantial rates of extra-pair paternity, which were ascribed to cuckoldry by bachelor males. Paternity shares of brood-tending males were consistently higher, and the numbers of sires per brood were consistently lower, in broods that were spawned in the dry seasons compared to broods from the rainy seasons. In contrast, the strength of size-assortative pairing in our V. moorii population did not vary temporally. Seasonal fluctuations in environmental conditions, such as water turbidity, are proposed as a mechanism behind variable cuckolder pressure. Our data demonstrate the utility of long-term monitoring to improve our understanding of animal mating patterns. Supplementary Information: The online version contains supplementary material available at 10.1007/s10750-022-05042-0.

The balance model of honest sexual signaling.

Costly signaling theory is based on the idea that individuals may signal their quality to potential mates and that the signal's costliness plays a crucial role in maintaining information content ("honesty") over evolutionary time. Although costly signals have traditionally been described as "handicaps," here we present mathematical results that motivate an alternative interpretation. We show that under broad conditions, the multiplicative nature of fitness selects for roughly balanced investments in mating success and viability, thereby generating a positive correlation between signal size and quality. This balancing tendency occurs because selection for increased investment in a fitness component diminishes with the absolute level of investment in that component, such that excessively biased investments are penalized. The resulting interpretation of costly signals as balanced (albeit not necessarily equal) investments may be a widely applicable alternative to the traditional "handicap" metaphor, which has been criticized for its non-Darwinian connotation of selection for "waste" rather than efficiency. We predict that accelerating returns on viability are necessary to undermine honesty. This prediction depends crucially on the assumption that mating success and viability contribute multiplicatively (rather than additively) to an individual's fitness.

Correlational selection in the age of genomics.

Ecologists and evolutionary biologists are well aware that natural and sexual selection do not operate on traits in isolation, but instead act on combinations of traits. This long-recognized and pervasive phenomenon is known as multivariate selection, or-in the particular case where it favours correlations between interacting traits-correlational selection. Despite broad acknowledgement of correlational selection, the relevant theory has often been overlooked in genomic research. Here, we discuss theory and empirical findings from ecological, quantitative genetic and genomic research, linking key insights from different fields. Correlational selection can operate on both discrete trait combinations and quantitative characters, with profound implications for genomic architecture, linkage, pleiotropy, evolvability, modularity, phenotypic integration and phenotypic plasticity. We synthesize current knowledge and discuss promising research approaches that will enable us to understand how correlational selection shapes genomic architecture, thereby linking quantitative genetic approaches with emerging genomic methods. We suggest that research on correlational selection has great potential to integrate multiple fields in evolutionary biology, including developmental and functional biology, ecology, quantitative genetics, phenotypic polymorphisms, hybrid zones and speciation processes.

Fisher's lost model of runaway sexual selection.

The bizarre elaboration of sexually selected traits such as the peacock's tail was a puzzle to Charles Darwin and his 19th century followers. Ronald A. Fisher crafted an ingenious solution in the 1930s, positing that female preferences would become genetically correlated with preferred traits due to nonrandom mating. These genetic correlations would translate selection for preferred traits into selection for stronger preferences, leading to a self-reinforcing process of ever-elaborating traits and preferences. It is widely believed that Fisher provided only a verbal model of this "runaway" process. However, in correspondence with Charles Galton Darwin, Fisher also laid out a simple mathematical model that purportedly confirms his verbal prediction of runaway sexual selection. Unfortunately, Fisher's model contains inconsistencies that render his quantitative conclusions inaccurate. Here, we correct Fisher's model and show that it contains all the ingredients of a working runaway process. We derive quantitative predictions of his model using numerical techniques that were unavailable in Fisher's time. Depending on parameter values, mean traits and preferences may increase until genetic variance is depleted by selection, exaggerate exponentially while their variances remain stable, or both means and variances may increase super-exponentially. We thus present the earliest mathematical model of runaway sexual selection.

Quantifying the causal pathways contributing to natural selection.

The consequences of natural selection can be understood from a purely statistical perspective. In contrast, an explicitly causal approach is required to understand why trait values covary with fitness. In particular, key evolutionary constructs, such as sexual selection, fecundity selection, and so on, are best understood as selection via particular fitness components. To formalize and operationalize these concepts, we must disentangle the various causal pathways contributing to selection. Such decompositions are currently only known for linear models, where they are sometimes referred to as "Wright's rules." Here, we provide a general framework, based on path analysis, for partitioning selection among its contributing causal pathways. We show how the extended selection gradient-which represents selection arising from a trait's causal effects on fitness-can be decomposed into path-specific selection gradients, which correspond to distinct causal mechanisms of selection. This framework allows for nonlinear effects and nonadditive interactions among variables, which may be estimated using standard statistical methods (e.g., generalized linear [mixed] models or generalized additive models). We thus provide a generalization of Wright's path rules that accommodates the nonlinear and nonadditive mechanisms by which natural selection commonly arises.

The evolution of gonad expenditure and gonadosomatic index (GSI) in male and female broadcast-spawning invertebrates.

Sedentary broadcast-spawning marine invertebrates, which release both eggs and sperm into the water for fertilization, are of special interest for sexual selection studies. They provide unique insight into the early stages of the evolutionary succession leading to the often-intense operation of both pre- and post-mating sexual selection in mobile gonochorists. Since they are sessile or only weakly mobile, adults can interact only to a limited extent with other adults and with their own fertilized offspring. They are consequently subject mainly to selection on gamete production and gamete success, and so high gonad expenditure is expected in both sexes. We review literature on gonadosomatic index (GSI; the proportion of body tissue devoted to gamete production) of gonochoristic broadcast spawners, which we use as a proxy for gonad expenditure. We show that such taxa most often have a high GSI that is approximately equal in both sexes. When GSI is asymmetric, female GSI usually exceeds male GSI, at least in echinoderms (the majority of species recorded). Intriguingly, though, higher male GSI also occurs in some species and appears more common than female-biased GSI in certain orders of gastropod molluscs. Our limited data also suggest that higher male GSI may be the prevalent pattern in sperm casters (where only males release gametes). We explore how selection might have shaped these patterns using game theoretic models for gonad expenditure that consider possible trade-offs with (i) somatic maintenance or (ii) growth, while also considering sperm competition, sperm limitation, and polyspermy. Our models of the trade-off between somatic tissue (which increases survival) and gonad (which increases reproductive success) predict that GSI should be equal for the two sexes when sperm competition is intense, as is probably common in broadcast spawners due to synchronous spawning in aggregations. Higher female GSI occurs under low sperm competition. Sperm limitation appears unlikely to alter these conclusions qualitatively, but can also act as a force to keep male GSI high, and close to that of females. Polyspermy can act to reduce male GSI. Higher male than female GSI is predicted to be less common (as observed in the data), but can occur when ova/ovaries are sufficiently more resource-intensive to produce than sperm/testes, for which some evidence exists. We also show that sex-specific trade-offs between gonads and growth can generate different life-history strategies for males and females, with males beginning reproduction earlier. This could lead to apparently higher male GSI in empirical studies if immature females are included in calculations of mean GSI. The existence of higher male GSI nonetheless remains somewhat problematic and requires further investigation. When sperm limitation is low, we suggest that the natural logarithm of the male/female GSI ratio may be a suitable index for sperm competition level in broadcast spawners, and that this may also be considered as an index for internally fertilizing taxa.