Sexual Selection Research Research Articles

Bateman (1948): pioneer in the measurement of sexual selection

Bateman (1948): pioneer in the measurement of sexual selection

Mate choice and sexual selection: What have we learned since Darwin?

Charles Darwin laid the foundation for all modern work on sexual selection in his seminal book The Descent of Man, and Selection in Relation to Sex. In this work, Darwin fleshed out the mechanism of sexual selection, a hypothesis that he had proposed in The Origin of Species. He went well beyond a simple description of the phenomenon by providing extensive evidence and considering the far-reaching implications of the idea. Here we consider the contributions of Darwin to sexual selection with a particular eye on how far we have progressed in the last 150 years. We focus on 2 key questions in sexual selection. First, why does mate choice evolve at all? And second, what factors determine the strength of mate choice (or intensity of sexual selection) in each sex? Darwin provided partial answers to these questions, and the progress that has been made on both of these topics since his time should be seen as one of the great triumphs of modern evolutionary biology. However, a review of the literature shows that key aspects of sexual selection are still plagued by confusion and disagreement. Many of these areas are complex and will require new theory and empirical data for complete resolution. Overall, Darwin's contributions are still surprisingly relevant to the modern study of sexual selection, so students of evolutionary biology would be well advised to revisit his works. Although we have made significant progress in some areas of sexual selection research, we still have much to accomplish.

The Evolution of Animal Weapons

Males in many species invest substantially in structures that are used in combat with rivals over access to females. These weapons can attain extreme proportions and have diversified in form repeatedly. I review empirical literature on the function and evolution of sexually selected weapons to clarify important unanswered questions for future research. Despite their many shapes and sizes, and the multitude of habitats within which they function, animal weapons share many properties: They evolve when males are able to defend spatially restricted critical resources, they are typically the most variable morphological structures of these species, and this variation honestly reflects among-individual differences in body size or quality. What is not clear is how, or why, these weapons diverge in form. The potential for male competition to drive rapid divergence in weapon morphology remains one of the most exciting and understudied topics in sexual selection research today.

Indirect mate choice, direct mate choice and species recognition in a bower‐building cichlid fish lek

Sexual selection arising through female mate choice typically favours males with larger, brighter and louder signals. A critical challenge in sexual selection research is to determine the degree to which this pattern results from direct mate choice, where females select individual males based on variation in signalling traits, or indirect mate choice, where male competition governs access to reproductively active females. We investigated female mate choice in a lekking Lake Malawi cichlid fish, Hemitilapia oxyrhynchus, in which males build and aggressively defend sand 'bowers'. Similar to previous studies, we found that male reproductive success was positively associated with bower height and centrality on the lek. However, this pattern resulted from males holding these territories encountering more females, and thus their greater success was due to indirect mate choice. Following initial male courtship, an increase in the relative mating success of some males was observed, but this relative increase was unrelated to bower size or position. Crucially, experimentally manipulating bowers to resemble those of a co-occurring species had no appreciable effect on direct choice by females or male spawning success. Together, these results suggest indirect mate choice is the dominant force determining male-mating success in this species, and that bowers are not signals used in direct mate choice by females. We propose that, in this species, bowers have a primary function in intraspecific male competition, with the most competitive males maintaining larger and more central bowers that are favoured by sexual selection due to higher female encounter rates.

Evolutionary Consequences of Sperm Cell Aging

Animal breeding research, reproductive biology, and cellular biogerontology show that fertilization rates and zygote viability critically depend on sperm age. Sexual selection research focuses on differences between male genotypes in sperm performance, such as motility, competitive ability, or compatibility with eggs, but without considering sperm age. A combined view (that the thermodynamically inevitable decline in sperm performance selects for traits in diploid individuals to prevent fertilization with aged sperm) has received very little attention. In this paper, I correct this bias and show that many male and female traits affect sperm aging or the sperm age distribution at any reproductive event. Such traits coincide well with condition-dependent traits considered sexually selected: multiple mating by both sexes, high sperm production rates, the delivery of dense ejaculates containing many sperm (including nonfertilizing types), the packaging of sperm into spermatophores, male and female sperm ejection, sexual coercion, as well as the production of showy antioxidants and various cellular and nuclear repair mechanisms. I conclude that altering the sperm age distribution at any step during reproduction can be an origin of sexually selected traits, and may explain presently observed paternity variation without assuming genetic incompatibility of gametes.

Contemporary evolution of secondary sexual traits in the wild

SummarySexual selection has been studied intensively, and is often strong in natural populations. Theoretical models, comparative studies and laboratory selection experiments all suggest that evolution driven by sexual selection should be rapid and common.However, there are relatively few documented cases of the contemporary evolution of secondary sexual traits in natural populations. Moreover, the causes are not always due to sexual selection, but often due to altered natural selection regimes, or an altered balance between natural and sexual selection.Here we discuss recent empirical studies that have demonstrated the contemporary evolution of secondary sexual traits in natural populations. Our examples include both continuous traits and discrete polymorphisms. Taxa in which the contemporary (rapid) evolution of secondary sexual traits have been demonstrated include fish, insects, mammals, reptiles and birds. The evolutionary rates of these changes range from 0·005 to 0·570 haldanes (arithmetic mean = 0·14; geometric mean = 0·095; median = 0·12).The relative rarity of examples could be explained by different genetic architectures of sexually selected traits compared with naturally selected traits, or by sexual selection regimes not being sustained in the long term. These factors could potentially slow down evolutionary rates of secondary sexual traits and make the detection of the contemporary evolution empirically more difficult.Promising and underutilized approaches to sexual selection research include reciprocal transplant experiments and estimation of sexual isolation between conspecific populations.

Color Signals in the Black Grouse (Tetrao tetrix): Signal Properties and Their Condition Dependency

Recent progress in techniques of quantifying between‐individual differences of color‐based ornaments has revealed undiscovered possibilities for research in sexual selection. We present how the color spectra data can be comprehensively used for studying the importance of sexual ornaments in the black grouse and how these ornaments are related to a male condition. For this, we used both correlative field and experimental data. Field data indicated that older males had more chromatic coloration than yearlings. Blue chroma of males was correlated with male mating success. We experimentally manipulated yearling birds with testosterone implants and found that testosterone‐implanted males had impaired expression of several sexual ornaments: 10 months after the implantation, both structural‐based blue and carotenoid‐based red eye comb coloration were diminished, as well as lyre (tail) length. However, the manipulation did not affect vital traits under natural selection (wing length or body mass). Our data indicate that structural color is an important trait in sexual selection in this lekking species. Importantly, the data also indicate that male sexual ornaments are more susceptible to environmental conditions than the other male traits, thus showing their heightened condition dependency compared with the other traits mediating the honesty of signaling.

Color Signals in the Black Grouse (Tetrao tetrix): Signal Properties and Their Condition Dependency

Recent progress in techniques of quantifying between-individual differences of color-based ornaments has revealed undiscovered possibilities for research in sexual selection. We present how the color spectra data can be comprehensively used for studying the importance of sexual ornaments in the black grouse and how these ornaments are related to a male condition. For this, we used both correlative field and experimental data. Field data indicated that older males had more chromatic coloration than yearlings. Blue chroma of males was correlated with male mating success. We experimentally manipulated yearling birds with testosterone implants and found that testosterone-implanted males had impaired expression of several sexual ornaments: 10 months after the implantation, both structural-based blue and carotenoid-based red eye comb coloration were diminished, as well as lyre (tail) length. However, the manipulation did not affect vital traits under natural selection (wing length or body mass). Our data indicate that structural color is an important trait in sexual selection in this lekking species. Importantly, the data also indicate that male sexual ornaments are more susceptible to environmental conditions than the other male traits, thus showing their heightened condition dependency compared with the other traits mediating the honesty of signaling.

Different sexual traits show covariation among genotypes: implications for sexual selection

An unresolved question in sexual selection research is whether different secondary sexual traits are developmentally independent or instead whether their degree of expression is a manifestation of a general resource pool (i.e., condition) within the organism. If degree of expression of different sexual traits reflects ability to accumulate condition, then covariation should exist across genotypes in the expression of these traits, even if they are very different in kind. Here we present evidence for predicted covariation between morphological (sex comb size) and behavioral (courtship song) sexual traits among genetic lines of Drosophila bipectinata Duda extracted from a natural population. There is evidence that both these traits in Drosophila are condition dependent and subject to sexual selection. We detected significant body size‐independent differences in comb size among 32 lines. Replicate lines exhibiting relatively high and low values of comb size were then subjected to analyses of courtship song. High sex comb lines exhibited shorter mean burst period and shorter mean burst duration than low sex comb lines. These song differences occurred only during the distant pursuit phase of male courtship and existed despite factoring out individual variations in sex comb size, the trait on the basis of which test lines were originally chosen. The results verify the prediction of an association between condition-dependent secondary sexual traits across genotypes and, therefore, support the existence of an overall genetic quality related to condition acquisition. Key words: condition, courtship song, Drosophila bipectinata, genetic quality, secondary sexual traits, sex comb. [Behav Ecol]

Sexual selection and mate choice

The past two decades have seen extensive growth of sexual selection research. Theoretical and empirical work has clarified many components of pre- and postcopulatory sexual selection, such as aggressive competition, mate choice, sperm utilization and sexual conflict. Genetic mechanisms of mate choice evolution have been less amenable to empirical testing, but molecular genetic analyses can now be used for incisive experimentation. Here, we highlight some of the currently debated areas in pre- and postcopulatory sexual selection. We identify where new techniques can help estimate the relative roles of the various selection mechanisms that might work together in the evolution of mating preferences and attractive traits, and in sperm-egg interactions.

THE ROLES OF NATURAL AND SEXUAL SELECTION DURING ADAPTATION TO A NOVEL ENVIRONMENT

The net effect of sexual selection on nonsexual fitness is controversial. On one side, elaborate display traits and preferences for them can be costly, reducing the nonsexual fitness of individuals possessing them, as well as their offspring. In contrast, sexual selection may reinforce nonsexual fitness if an individual's attractiveness and quality are genetically correlated. According to recent models, such good-genes mate choice should increase both the extent and rate of adaptation. We evolved 12 replicate populations of Drosophila serrata in a powerful two-way factorial experimental design to test the separate and combined contributions of natural and sexual selection to adaptation to a novel larval food resource. Populations evolving in the presence of natural selection had significantly higher mean nonsexual fitness when measured over three generations (13-15) during the course of experimental evolution (16-23% increase). The effect of natural selection was even more substantial when measured in a standardized, monogamous mating environment at the end of the experiment (generation 16; 52% increase). In contrast, and despite strong sexual selection on display traits, there was no evidence from any of the four replicate fitness measures that sexual selection promoted adaptation. In addition, a comparison of fitness measures conducted under different mating environments demonstrated a significant direct cost of sexual selection to females, likely arising from some form of male-induced harm. Indirect benefits of sexual selection in promoting adaptation to this novel resource environment therefore appear to be absent in this species, despite prior evidence suggesting the operation of good-genes mate choice in their ancestral environment. How novel environments affect the operation of good-genes mate choice is a fundamental question for future sexual selection research.

Sexual selection research on spiders: progress and biases

The renaissance of interest in sexual selection during the last decades has fuelled an extraordinary increase of scientific papers on the subject in spiders. Research has focused both on the process of sexual selection itself, for example on the signals and various modalities involved, and on the patterns, that is the outcome of mate choice and competition depending on certain parameters. Sexual selection has most clearly been demonstrated in cases involving visual and acoustical signals but most spiders are myopic and mute, relying rather on vibrations, chemical and tactile stimuli. This review argues that research has been biased towards modalities that are relatively easily accessible to the human observer. Circumstantial and comparative evidence indicates that sexual selection working via substrate-borne vibrations and tactile as well as chemical stimuli may be common and widespread in spiders. Pattern-oriented research has focused on several phenomena for which spiders offer excellent model objects, like sexual size dimorphism, nuptial feeding, sexual cannibalism, and sperm competition. The accumulating evidence argues for a highly complex set of explanations for seemingly uniform patterns like size dimorphism and sexual cannibalism. Sexual selection appears involved as well as natural selection and mechanisms that are adaptive in other contexts only. Sperm competition has resulted in a plethora of morphological and behavioural adaptations, and simplistic models like those linking reproductive morphology with behaviour and sperm priority patterns in a straightforward way are being replaced by complex models involving an array of parameters. Male mating costs are increasingly being documented in spiders, and sexual selection by male mate choice is discussed as a potential result. Research on sexual selection in spiders has come a long way since Darwin, whose spider examples are reanalysed in the context of contemporary knowledge, but the same biases and methodological constraints have persisted almost unchanged through the current boom of research.

Reproductive Consequences of Population Divergence through Sexual Conflict

Sexual-selection research increasingly focuses on reproductive conflicts between the sexes [1–4]. Sexual conflict, divergent evolutionary interests of males and females [5], can cause rapid antagonistic coevolution of reproductive traits [6] and is a potentially powerful speciation engine [7–11]. This idea has theoretical and comparative support [10–12] but remains controversial [13–14]. Recent experimental evidence from Sepsis cynipsea indicates that populations with greater sexual conflict diverged more quickly; females were less likely to mate with males from other populations when flies had evolved under high levels of sexual conflict [15]. The consequences of this divergence have not been addressed, so here we assess two female fitness surrogates after 44 generations of evolving (and diverging) under three different levels of sexual conflict. Longevity after copulation was negatively associated with the degree of sexual conflict under which flies evolved, and housing females with males also reduced female longevity. Female lifetime reproductive success (LRS) also tended to decrease with increasing conflict. However, there was evidence of either sexual-selection fitness benefits at intermediate levels of sexual selection and conflict or inbreeding depression in the smallest populations (those with the lowest levels of conflict). Nevertheless, the results indicate that there can be a fitness load associated with sexual selection [2] and support claims that sexual conflict can lead to reproductive isolation [7–11, 15].

DO THE Imates HAVE IT?1

One of Darwin's great insights, sexual selection as an explanation for sexual differences, simmered for almost 100 years before blossoming into an active area of inquiry in the late 20th century. A major review of theory and evidence came with Malte Andersson's (1994) Sexual Selection. Mating Systems and Strategies is in the same Behavior and Ecology series as the earlier volume. However, its purpose is not to review but instead to establish a more rigorous approach to sexual selection research. Shuster and Wade describe a method to quantify the opportunity for sexual selection, a process that is usually more intense on males and is strongly influenced by the spatial and temporal distribution of mates. The authors also present a very critical examination of current behavioral-ecological concepts that apply to sexual selection. A major chapter reclassifies mating systems in animals, described with regard to the typical number of matings per male or female (e.g., monogamy). Shuster and Wade's proposal to measure sexual selection begins with the simple observation that males vary more than females in their number of mates; some males copulate often but others remain chaste. A statistical measure of this variation, Imates' forms the book's foundation. Why bother and other criticisms of earlier versions of this methodology (Bradbury and Andersson 1987) are tackled in Chapter 1. Shuster and Wade suggest that measuring sexual selection is the way to address an apparent paradox: What sort of processes, operating in only one sex, could possibly produce what appears to be one of the most rapidly evolving types of traits-the remarkably large differences in male ornamentation and sexual displays observed in closely related species? Using the degree of sexual dimorphism in ornaments, researchers should be able to predict the strength of sexual selection and the form of mating system for any given animal species. The dimensionless nature of Imates should fit the bill perfectly for making comparisons between species. The Imates approach may well turn out to be helpful and practical (more on this below) but Shuster and Wade do little in the way of promoting the merits of their method over other published schemes for measuring sexual selection (a tendency to disregard alternative viewpoints crops up throughout the book, including the sections that are critical of theory). There is no direct comparison of methods, of the sort for example, conducted by Fairbairn and Wilby (2001), who

THE STUDY OF INTERSEXUAL SELECTION USING QUANTITATIVE GENETICS

AbstractIn this review, I stress the importance of incorporating Quantitative Genetics (QG) in the study of sexual selection through female mate choice. A short overview of QG principles and methods of estimating genetic variance and covariance is given. The state of knowledge is summarized as to two QG assumptions (genetic variance in female mating preferences and male sexual traits) and one QG prediction (genetic covariance between preferences and preferred traits) of models of sexual selection. A review is given of studies of repeatability of mating preferences because of recent accumulation of data. The general conclusion is that sexual traits and mating preferences show large genetic variation and are genetically correlated. The extensive genetic variation asks for an explanation that goes beyond the ususal explanations of the maintenance of genetic variation in fitness traits. Two models that explain the high genetic variance in sexual traits are treated in detail: modifier selection and condition dependence. There are many unexplored areas of QG research that could stimulate further research in sexual selection like the study of genetic covariance between mating preferences and good genes, of genetic variances and covariances of multiple male traits and multiple females preferences, of genetic variance in condition, and of condition dependence of mating preferences.

Pollen Removal, Paternity, and the Male Function of Flowers

Much recent research suggests that floral characteristics of hermaphroditic plants are often selected primarily because of their effects on male reproduction. Two recent challenges to this view have been based on the fate of pollen after it is removed by pollinators, something that is rarely measured in field studies. One objection is theoretical, holding that the large variance in the success of pollen after it is removed weakens selection through the male side (Wilson et al. 1994). The other objection is empirical. In a species in which pollen removal studies had suggested that flowers are primarily male, new paternity data have been used to argue that they are not (Broyles and Wyatt 1990a, 1990b, 1995). Here I argue that both objections are invalid, the theoretical argument because it uses the wrong measure of selection, and the empirical study because a confounding variable was not controlled. Bateman (1948) provided a foundation for understanding why males often act as if they take a greater interest in having many mates than females do. This difference arises because of an asymmetry in reproductive costs. Males commonly invest little or nothing in offspring, whereas female investment may be large. Therefore, reproductive success of females is limited by resources, and mating frequently has comparatively little effect on their fitness, whereas male success is limited by access to females and may increase linearly with the number of mates. Bateman's principle helped fuel an explosion of interest in sexual selection in animals, recently summarized by Andersson (1994). Bateman believed his principle to be nearly universal and explicitly included plants among the relevant organisms. However, sexual selection research on plants lagged behind that on animals, partly for historical reasons and perhaps partly because it was unclear how to apply the ideas to hermaphroditic organisms that were both male and female (reviewed in Willson 1994). It was eventually recognized how Bateman's principle might apply to these organisms (e.g., Charnov 1979; Wilson 1979; Willson and Burley 1983). For example, consider an animal-pollinated hermaphroditic plant. It needs to attract pollinators for two reasons: to receive pollen for its own seed (female function) and to have its pollen

Sexual Selection and Variance in Reproductive Success

Sexual Selection and Variance in Reproductive Success