Jonathan M. Henshaw

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

Significance How does sexual selection differ between males and females? What is its role in the speciation process? Answering such questions requires a reliable method to measure sexual selection, so that we can compare its strength between the sexes and across taxa. The development of appropriate measures has led to sustained controversy, however, with no measure being widely accepted. We provide to our knowledge the first rigorous comparison of indexes of sexual selection. Our results unambiguously support the use of a recently defined measure, the Jones index, over more established indexes of sexual selection such as the Bateman gradient. 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.

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.

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.

Bet-hedging via polyandry: a comment on 'Mating portfolios: bet-hedging, sexual selection and female multiple mating'.

Garcia-Gonzalez et al. [[1][1]] conducted an original and elegant experiment examining whether fertilization of a females eggs by multiple males (polyandry) can provide fitness benefits via ‘bet-hedging’ (i.e. due to decreased variance in offspring fitness). The authors measured these benefits

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).

A unified measure of linear and nonlinear selection on quantitative traits

1.Lande and Arnolds approach to quantifying natural selection has become a standard tool in evolutionary biology due to its simplicity and generality. It treats linear and nonlinear selection in two separate frameworks, generating coefficients of selection (e.g. linear and quadratic selection gradients) that are not directly comparable. Due to this somewhat artificial division, the Lande-Arnold approach lacks an integrated measure of the strength of selection that applies across qualitatively different selection regimes (e.g. directional, stabilizing, or disruptive selection). 2.We define a unified measure of selection, the distributional selection differential (DSD), which includes both linear and nonlinear selection. The DSD quantifies total selection on a trait, regardless of the underlying selection regime. 3.The DSD can be partitioned into a directional component, representing selection on the trait mean, and a nondirectional component, representing selection on the shape of the trait distribution (e.g. variance, skew, or the number of modes). When multiple traits are measured, the DSD can also be separated into direct and correlated effects, analogously to linear selection gradients. As with linear selection differentials, the DSD on a standardized trait is limited in magnitude by the opportunity for selection. 4.The DSD is a general-purpose measure of the total strength of selection. It is particularly valuable where traditional analyses provide limited insight, such as in comparative studies where the shape of selection is variable. Partitioning the DSD into directional and nondirectional selection allows biologists to assess whether selection acts consistently in one direction, or in opposing directions over different parts of the trait range. This article is protected by copyright. All rights reserved.

The Economics of Egg Trading: Mating Rate, Sperm Competition and Positive Frequency-Dependence

Egg trading—the alternating exchange of egg parcels during mating by simultaneous hermaphrodites—is one of the best-documented examples of reciprocity between non-relatives. By offering eggs only to partners who reciprocate, traders increase their reproductive success in the male role, but at a potential cost of delaying or reducing fertilisation of their own eggs. Although several authors have considered the evolutionary stability of egg trading once it has evolved, little attention has been paid to how egg trading can invade a population in the first place. We begin to tackle this problem by formally showing that egg trading is under positive frequency-dependent selection: once the proportion of traders in a population exceeds a certain threshold, egg trading will go to fixation. We show that if mate encounters occur frequently, then the cost of withholding eggs from unreciprocating partners is reduced, making it easier for egg trading to evolve. In contrast, the presence of opportunistic ‘streaking’, where unpaired individuals join mating pairs but contribute only sperm, makes it more difficult for egg trading to invade. This is because streakers weaken the link between the number of eggs an individual can offer and its male-role reproductive success.

Direct reciprocity stabilizes simultaneous hermaphroditism at high mating rates: A model of sex allocation with egg trading

Simultaneous hermaphroditism is predicted to be unstable at high mating rates given an associated increase in sperm competition. The existence of reciprocal egg trading, which requires both hermaphroditism and high mating rates to evolve, is consequently hard to explain. We show using mathematical models that the presence of a trading economy creates an additional fitness benefit to egg production, which selects for traders to bias their sex allocation toward the female function. This female‐biased sex allocation prevents pure females from invading a trading population, thereby allowing simultaneous hermaphroditism to persist stably at much higher levels of sperm competition than would otherwise be expected. More generally, our model highlights that simultaneous hermaphroditism can persist stably when mating opportunities are abundant, as long as sperm competition remains low. It also predicts that reciprocity will select for heavier investment in the traded resource.

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.

How to quantify (the response to) sexual selection on traits: HOW TO QUANTIFY SEXUAL SELECTION

Natural selection operates via fitness components like mating success, fecundity, and longevity, which can be understood as intermediaries in the causal process linking traits to fitness. In particular, sexual selection occurs when traits influence mating or fertilization success, which, in turn, influences fitness. We show how to quantify both these steps in a single path analysis, leading to better estimates of the strength of sexual selection. Our model controls for confounding variables, such as body size or condition, when estimating the relationship between mating and reproductive success. Correspondingly, we define the Bateman gradient and the Jones index using partial rather than simple regressions, which better captures how they are commonly interpreted. The model can be applied both to purely phenotypic data and to quantitative genetic parameters estimated using information on relatedness. The phenotypic approach breaks down selection differentials into a sexually selected and a “remainder” component. The quantitative genetic approach decomposes the estimated evolutionary response to selection analogously. We apply our method to analyze sexual selection in male dusky pipefish, Syngnathus floridae, and in two simulated datasets. We highlight conceptual and statistical limitations of previous path‐based approaches, which can lead to substantial misestimation of sexual selection.