Intensity Of Sexual Selection Research Articles

Sexual selection, germline mutation rate and sperm competition

BackgroundAn important component of sexual selection arises because females obtain viability benefits for their offspring from their mate choice. Females choosing extra-pair fertilization generally favor males with exaggerated secondary sexual characters, and extra-pair paternity increases the variance in male reproductive success. Furthermore, females are assumed to benefit from 'good genes' from extra-pair sires. How additive genetic variance in such viability genes is maintained despite strong directional selection remains an evolutionary enigma. We propose that sexual selection is associated with elevated mutation rates, changing the balance between mutation and selection, thereby increasing variance in fitness and hence the benefits to be obtained from good genes sexual selection. Two hypotheses may account for such elevated mutation: (1) Increased sperm production associated with sperm competition may increase mutation rate. (2) Mutator alleles increase mutation rates that are revealed by the expression of condition-dependent secondary sexual characters used by choosy females during their mate choice. M Petrie has independently developed the idea that mutator alleles may account for the maintenance of genetic variation in viability despite strong directional selection.ResultsA comparative study of birds revealed a positive correlation between mutation rate at minisatellite loci and extra-pair paternity, but not between mutation rate and relative testes mass which is a measure of relative sperm production. Minisatellite mutation rates were not related to longevity, suggesting a meiotic rather than a mitotic origin of mutations.ConclusionWe found evidence of increased mutation rate in species with more intense sexual selection. Increased mutation was not associated with increased sperm production, and we suggest that species with intense sexual selection may maintain elevated mutation rates because sexual selection continuously benefits viability alleles expressed in condition-dependent characters. Sexual selection may increase mutational input, which in turn feeds back on sexual selection because of increased variance in viability traits.

Population Structure and Operational Sex Ratio in the Rock Shrimp Rhynchocinetes Typus (Decapoda: Caridea)

The ratio of sexually active males to fertilizable females (operational sex ratio, OSR) is the most important parameter determining the direction and intensity of sexual selection. It is widely accepted that the pronounced sexual dimorphism featured by many crustaceans is a consequence of a strongly malebiased OSR. Many studies have contributed to the understanding of function and origin of sexually selected traits, but few attempts have been made to measure the OSR. Using the rock shrimp Rhynchocinetes typus as an example, herein we propose a relatively simple method to assess the OSR of natural populations of crustaceans, as follows. The number of individuals willing to mate was estimated by the study of both the population structure (field sampling) and the readiness to mate (laboratory experiments). Field sampling showed that adult sex ratio was balanced during most seasons and that early ontogenetic male stages dominated among the males. Laboratory experiments demonstrated that females became receptive asynchronously, and that males from early ontogenetic stages showed limited readiness to mate. Based on this information, we estimated the OSR under three different scenarios. The results indicate that the OSR is highly male-biased in R. typus even in the more conservative scenario supporting the original predictions. Most male mate-competitors are early ontogenetic stages, whereas few are late stages. The results demonstrate the importance of estimating the OSR individually for shrimp categories differing primarily by sex and subsequently by individual conditions (ontogenetic stage, molt stage), which affects the probability of a potential mate to be sexually active. We suggest that this approach provides important information necessary for a better understanding of crustacean mating systems.

MICROSATELLITE DNA EVIDENCE FOR GENE FLOW IN NEOTROPICAL LEK-MATING LONG-TAILED MANAKINS

Abstract I genotyped lek-mating Long-tailed Manakins (Chiroxiphia linearis) at Monteverde and Santa Rosa, Costa Rica, 115 km apart. Cavalli-Sforza distance was 0.04, DLR was 0.18, and RST and θ were both 0.02. Bayesian clustering analysis indicated that both populations were part of a single cluster rather than from distinct clusters. I present a binomial test for probability of allelic absence as a function of sample size. Genotypic likelihood tests assigned 50% of Monteverde birds to Santa Rosa, versus 26% of Santa Rosa birds to Monteverde. Two lines of evidence supported the idea of asymmetric gene flow up the elevational gradient from Santa Rosa to Monteverde. Low differentiation at this spatial scale, despite intense sexual selection, suggests that sexual selection alone is unlikely to promote rapid divergence leading to speciation. Reduced gene flow, produced by geographic barriers or behavioral factors, may also be required. Evidencia de Flujo Genico Mediante ADN Microsatelital en Chiroxiphia linea...

Geographic variation in sexual selection among populations of an iguanid lizard, Sauromalus obesus (=ater).

Geographic variation in selection pressures may result in population divergence and speciation, especially if sexual selection varies among populations. Yet spatial variation in targets and intensity of sexual selection is well studied in only a few species. Even more rare are simultaneous studies of multiple populations combining observations from natural settings with controlled behavioral experiments. We investigated how sexual selection varies among populations of the chuckwalla, Sauromalus obesus. Chuckwallas are sexually dimorphic in color, and males vary in coloration among populations. Using field observations and multiple regression techniques, we investigated how sexual selection acts on various male traits in three populations in which males differed in coloration. The influence of sexual selection on male coloration was then investigated in more detail using controlled experiments. Results from field observations indicate that phenotypic selection was acting on territory quality in all three populations. In two populations, selection was also acting either directly or indirectly on male coloration. Male color likely functions as an indicator of food resources to females because male color is based partly on carotenoid pigments. In controlled experiments, significantly more females from these two populations chose males with brighter colors over dull males, a result consistent with studies on carotenoid pigments in other taxa. In a third population, no evidence of sexual selection on male coloration was found in either the field study or controlled experiment. Lack of female preferences for male color in this population, in which chuckwalla densities are low and home ranges are large, may result from searching costs to females.

Understanding Reversals in the Relative Strength of Sexual Selection on Males and Females: A Role for Sperm Competition?

Sperm competition affects sexual selection intensity on males, but models suggest it cannot affect the relative intensity of sexual selection on males compared to females. However, if sperm competition depresses the payoff for male multiple mating, it could affect the relative intensity of sexual selection and even cause sexual selection to be more intense on females than males (reversal of typical pattern). To evaluate how sperm competition, energy availability, and parental investment affect the intensity of sexual selection on each sex, I constructed a simulation model using the relationship between fecundity and number of mates to estimate sexual selection gradients. Unlike earlier models, I include a trade-off between paternal investment and sperm competition ability. The amount of energy available for reproduction affects the sexual selection gradient for each sex. Reversals in the sex experiencing stronger sexual selection do occur when additional paternal investment reduces a male's ability to compete for fertilizations within females. The shape of the distribution of mates for each sex (determined by mate competition) is also important. Output from the model is qualitatively similar to empirical data from insects with paternal investment. This model challenges previous thinking about the role of sperm competition in sex-role reversal.

Nuptial gifts and the evolution of male body size.

In many insect systems, males donate nuptial gifts to insure an effective copulation or as a form of paternal investment. However, if gift magnitude is both body size-limited and positively related to fitness, then the opportunity exists for the gift to promote the evolution of large male size. In the striped ground cricket, Allonemobius socius, males transfer a body size-limited, somatic nuptial gift that is comprised primarily of hemolymph. To address the implications of this gift on male size evolution, we quantified the intensity and direction of natural (fecundity) and sexual (mating success) selection over multiple generations. We found that male size was under strong positive sexual selection throughout the breeding season. This pattern of selection was similar in successive generations spanning multiple years. Male size was also under strong natural selection, with the largest males siring the most offspring. However, multivariate selection gradients indicated that gift size, and not male size, was the best predictor of female fecundity. In other words, direct fecundity selection for larger gifts placed indirect positive selection on male body size, supporting the hypothesis that nuptial gifts can influence the evolution of male body size in this system. Although female size was also under strong selection due to a size related fecundity advantage, it did not exceed selection on male size. The implications of these results with regard to the maintenance of the female-biased size dimorphic system are discussed.

POPULATION VARIATION IN SEXUAL SELECTION AND ITS EFFECT ON SIZE ALLOMETRY IN TWO DUNG FLY SPECIES WITH CONTRASTING SEXUAL SIZE DIMORPHISM

Body size is one of the most important quantitative traits under evolutionary scrutiny. Sexual size dimorphism (SSD) in a given species is expected to result if opposing selection forces equilibrate differently in both sexes. We document variation in the intensity of sexual and fecundity selection, male and female body size, and thus SSD among 31 and 27 populations of the two dung fly species, Scathophaga stercoraria and Sepsis cynipsea, across Switzerland. Whereas in S. cynipsea females are larger, the SSD is reversed in S. stercoraria. We comprehensively evaluated Fairbairn and Preziosi's (1994) general, three-tiered scenario, hypothesizing that sexual selection for large male size is the major driving force of SSD allometry within these two species. Sexual selection intensity on male size in the yellow dung fly, S. stercoraria, was overall positive, greater, and more variable among populations than fecundity selection on females. Also, sexual selection intensity in a given population correlated positively with mean male body size of that population for both the field-caught fathers and their laboratory-reared sons, indicating a response to selection. In S. cvnipsea, sexual selection intensity on males was lower overall and significantly positive, about equal in magnitude, but more variable than fecundity selection on females. However, there was no correlation between the intensity of sexual selection and mean male body size among populations. In both species, the laboratory-reared offspring indicate genetic differentiation among populations in body size. Despite fulfillment of all key prerequisites, at least in S. stercoraria, we did not find hypoallometry for SSD (Rensch's rule, i.e., greater evolutionary divergence in male size than female size) for the field-caught parents or the laboratory-reared offspring: Female size was isometric to male size in both species. We conclude that S. cynipsea does not fit some major requirements of Fairbairn and Preziosi's (1994) scenario, whereas for S. stercoraria we found partial support for it. Failure to support Rensch's rule within the latter species may be due to phylogenetic or other constraints, power limitations, erroneous estimates of sexual selection, insufficient genetic isolation of populations, or sex differences in viability selection against large size.

GEOGRAPHIC VARIATION IN SEXUAL SELECTION AMONG POPULATIONS OF AN IGUANID LIZARD, SAUROMALUS OBESUS (=ATER)

Geographic variation in selection pressures may result in population divergence and speciation, especially if sexual selection varies among populations. Yet spatial variation in targets and intensity of sexual selection is well studied in only a few species. Even more rare are simultaneous studies of multiple populations combining observations from natural settings with controlled behavioral experiments. We investigated how sexual selection varies among populations of the chuckwalla, Sauromalus obesus. Chuckwallas are sexually dimorphic in color, and males vary in coloration among populations. Using field observations and multiple regression techniques, we investigated how sexual selection acts on various male traits in three populations in which males differed in coloration. The influence of sexual selection on male coloration was then investigated in more detail using controlled experiments. Results from field observations indicate that phenotypic selection was acting on territory quality in all three populations. In two populations, selection was also acting either directly or indirectly on male coloration. Male color likely functions as an indicator of food resources to females because male color is based partly on carotenoid pigments. In controlled experiments, significantly more females from these two populations chose males with brighter colors over dull males, a result consistent with studies on carotenoid pigments in other taxa. In a third population, no evidence of sexual selection on male coloration was found in either the field study or controlled experiment. Lack of female preferences for male color in this population, in which chuckwalla densities are low and home ranges are large, may result from searching costs to females.

NUPTIAL GIFTS AND THE EVOLUTION OF MALE BODY SIZE

In many insect systems, males donate nuptial gifts to insure an effective copulation or as a form of paternal investment. However, if gift magnitude is both body size-limited and positively related to fitness, then the opportunity exists for the gift to promote the evolution of large male size. In the striped ground cricket, Allonemobius socius, males transfer a body size-limited, somatic nuptial gift that is comprised primarily of hemolymph. To address the implications of this gift on male size evolution, we quantified the intensity and direction of natural (fecundity) and sexual (mating success) selection over multiple generations. We found that male size was under strong positive sexual selection throughout the breeding season. This pattern of selection was similar in successive generations spanning multiple years. Male size was also under strong natural selection, with the largest males siring the most offspring. However, multivariate selection gradients indicated that gift size, and not male size, was the best predictor of female fecundity. In other words, direct fecundity selection for larger gifts placed indirect positive selection on male body size, supporting the hypothesis that nuptial gifts can influence the evolution of male body size in this system. Although female size was also under strong selection due to a size related fecundity advantage, it did not exceed selection on male size. The implications of these results with regard to the maintenance of the female-biased size dimorphic system are discussed.Corresponding Editor: S. Pitnick

Genetic evidence for extreme polyandry and extraordinary sex-role reversal in a pipefish.

Due to the phenomenon of male pregnancy, the fish family Syngnathidae (seahorses and pipefishes) has historically been considered an archetypal example of a group in which sexual selection should act more strongly on females than on males. However, more recent work has called into question the idea that all species with male pregnancy are sex-role reversed with respect to the intensity of sexual selection. Furthermore, no studies have formally quantified the opportunity for sexual selection in any natural breeding assemblage of pipefishes or seahorses in order to demonstrate conclusively that sexual selection acts most strongly on females. Here, we use a DNA-based study of parentage in the Gulf pipefish Syngnathus scovelli in order to show that sexual selection indeed acts more strongly on females than on males in this species. Moreover, the Gulf pipefish exhibits classical polyandry with the greatest asymmetry in reproductive roles (as quantified by variances in mating success) between males and females yet documented in any system. Thus, the intensity of sexual selection on females in pipefish rivals that of any other taxon yet studied.

Predation risk reduces male-male sexual competition in the Trinidadian guppy ( Poecilia reticulata )

Because agonistic behaviour can increase an individual's risk of predation, natural selection should favour individuals that modify their behaviour in the face of predation hazard in ways that maximise fitness. We investigated experimentally the effects of an increase in the apparent risk of predation on male-male competition within mixed-sex shoals of the Trinidadian guppy (Poecilia reticulata). We show that males engaged in significantly fewer aggressive interactions with conspecific males in the presence of a fish predator. However, they continued to court and attempt copulations with females at the same rate irrespective of the level of predation risk. In comparison, under predation hazard, female guppies were less responsive sexually and avoided fewer male copulation attempts. Such predator-mediated changes in male-male agonistic interactions and female sexual responsiveness towards males have important implications for the mode and intensity of sexual selection within populations.

Sex Chromosome Meiotic Drive

▪ Abstract Sex chromosome drive refers to the unequal transmission of X and Y chromosomes from individuals of the heterogametic sex, resulting in biased sex ratios among progeny and within populations. The presence of driving sex chromosomes can reduce mean fitness within a population, bring about intragenomic conflict between the X chromosome, the Y, and the autosomes, and alter the intensity or mode of sexual selection within species. Sex chromosome drive, or its genetic equivalent, is known in plants, mammals, and flies. Many species harboring driving X chromosomes have evolved Y-linked and autosomal suppressors of drive. If a drive polymorphism is not stable, then driving chromosomes may spread to fixation and cause the extinction of a species. Certain characteristics of species, such as population density and female mating rate, may affect the probability of fixation of driving chromosomes. Thus, sex chromosome drive could be an agent of species-level selection.

EVOLUTION OF LIFE HISTORIES ALONG ELEVATIONAL GRADIENTS: TRADE-OFF BETWEEN PARENTAL CARE AND FECUNDITY

Life history responses to environmental conditions include a combination of fecundity-survival schedules and behavioral strategies that yield the highest fitness in a given environment. In this study, we examined the pattern of covariation in avian life history strategies along an elevational gradient by comparing variation in life history traits, including most components of parental care, between phylogenetically paired taxa from low- and high-elevation sites. We found that high-elevation species had significantly lower annual fecundity but provided greater parental care to their offspring. However, a strong negative relationship between offspring number and duration of parental care along the elevational gradient suggested that high-elevation species were shifting investment from offspring number toward offspring quality. Although adult survival did not differ between high- and low-elevation species, higher juvenile survival may have compensated for lower annual fecundity in high-elevation species. The elevation at which breeding occurred strong- ly influenced the partitioning of parental behavior between sexes. Male participation in nestling provisioning was significantly greater in high-elevation species. In turn, altitudinal variation in the frequency of biparental care closely covaries with the intensity of sexual selection, ultimately resulting in the strong elevational pattern of sexual dimorphism. More- over, elevational variation in costs of development and maintenance of secondary sexual traits constitutes an additional effect on fecundity-survival schedules along elevational gradients. Thus, a trade-off between fecundity and parental care, and associated interactions among morphological, life history, and behavioral traits play important roles in the evolution of life history strategies in birds.

Is the bat os penis sexually selected?

The mammalian os penis or baculum is an extremely diverse bone but our understanding of the selective forces behind this diversity remains poor. While genital morphology is generally assumed to be sexually selected, there have been relatively few attempts to test this hypothesis. Here we investigate associations between baculum length and two measures of sexual selection intensity (mating system and testis mass) across bats. Analyses were conducted using both species-level data and phylogenetic comparative techniques. Controlling for the effect of male body mass, baculum length was positively associated with relative testis mass in all cross-species analyses. Additionally, in an analysis that also included mating system, there was an interaction between testis mass, body mass and mating system that significantly influenced baculum length. However, after using independent contrasts to control for phylogenetic inertia in these data, baculum length was not significantly associated with mating system, testis mass or body mass. Thus, increased length of the baculum in bats appears not to be associated with increased sperm competition risk or sexual selection intensity.

Female guppies agree to differ: phenotypic and genetic variation in mate-choice behavior and the consequences for sexual selection.

Variation among females in mate choice may influence evolution by sexual selection. The genetic basis of this variation is of interest because the elaboration of mating preferences requires additive genetic variation in these traits. Here we measure the repeatability and heritability of two components of female choosiness (responsiveness and discrimination) and of female preference functions for the multiple ornaments borne by male guppies (Poecilia reticulata). We show that there is significant repeatable variation in both components of choosiness and in some preference functions but not in others. There appear to be several male ornaments that females find uniformly attractive and others for which females differ in preference. One consequence is that there is no universally attractive male phenotype. Only responsiveness shows significant additive genetic variation. Variation in responsiveness appears to mask variation in discrimination and some preference functions and may be the most biologically relevant source of phenotypic and genetic variation in mate-choice behavior. To test the potential evolutionary importance of the phenotypic variation in mate choice that we report, we estimated the opportunity for and the intensity of sexual selection under models of mate choice that excluded and that incorporated individual female variation. We then compared these estimates with estimates based on measured mating success. Incorporating individual variation in mate choice generally did not predict the outcome of sexual selection any better than models that ignored such variation.

How cuckoldry can decrease the opportunity for sexual selection: data and theory from a genetic parentage analysis of the sand goby, Pomatoschistus minutus.

Alternative mating strategies are common in nature and are generally thought to increase the intensity of sexual selection. However, cuckoldry can theoretically decrease the opportunity for sexual selection, particularly in highly polygamous species. We address here the influence of sneaking (fertilization thievery) on the opportunity for sexual selection in the sand goby Pomatoschistus minutus, a marine fish species in which males build and defend nests. Our microsatellite-based analysis of the mating system in a natural sand goby population shows high rates of sneaking and multiple mating by males. Sneaker males had fertilized eggs in approximately 50% of the assayed nests, and multiple sneakers sometimes fertilized eggs from a single female. Successful males had received eggs from 2 to 6 females per nest (mean = 3.4). We developed a simple mathematical model showing that sneaking in this polygynous sand goby population almost certainly decreases the opportunity for sexual selection, an outcome that contrasts with the usual effects of cuckoldry in socially monogamous animals. These results highlight a more complex and interesting relationship between cuckoldry rates and the intensity of sexual selection than previously assumed in much of the literature on animal mating systems.

The genetic mating system and tests for cuckoldry in a pipefish species in which males fertilize eggs and brood offspring externally.

Highly variable microsatellite loci were used to study the mating system of Nerophis ophidion, a species of pipefish in which pregnant males carry embryos on the outside of their body rather than in an enclosed brood pouch. Despite this mode of external fertilization and brooding, otherwise rare in the family Syngnathidae, the genotypes of all embryos proved to be consistent with paternity by the tending male, thus indicating that cuckoldry by sneaker males is rare or nonexistent in this species. N. ophidion is a phylogenetic outlier within the Syngnathidae and its reproductive morphology is thought to be close to the presumed ancestral condition for pipefishes and seahorses. Thus, our genetic results suggest that the evolutionary elaboration of the enclosed brood pouch elsewhere in the family was probably not in response to selection pressures on pregnant males to avoid fertilization thievery. With regard to maternity assignments, our genotypic data are consistent with behavioural observations indicating that females sometimes mate with more than one male during a breeding episode, and that each male carries eggs from a single female. Thus, the polyandrous genetic mating system in this species parallels the social mating system, and both are consistent with a more intense sexual selection operating on females, and the elaboration of secondary sexual characters in that gender.

Sexual selection and the geography of Plasmodium infection in Savannah sparrows (Passerculus sandwichensis).

According to Hamilton and Zuk's hypothesis of parasite-mediated sexual selection, host-parasite coevolution maintains variation in male genetic quality and allows for strong intersexual selection in species with high rates of infection. In birds, most interspecific tests of this hypothesis relate the prevalence of blood parasites to some measure of the intensity of sexual selection. Such tests often rely on limited sampling of single populations to estimate species-wide infection rates, and many tests are thus vulnerable to intraspecific (geographic) variation in the evolutionary ecology of disease. Here, we used molecular techniques to examine variation in the prevalence of Plasmodium spp. across 14 populations of Savannah sparrows, Passerculus sandwichensis, in eastern North America. Plasmodium could not be detected in any of 68 island birds, but 34 of 119 (29%) mainland males, and 7 of 43 (16%) mainland females were infected. Among mainland birds, infection was common in southern populations but rare in New Brunswick, Canada. Overall, the prevalence of Plasmodium ranged from 0 to 60% across populations, although only 17.8% of birds were infected in the pooled (species-wide) sample. The extent of this geographic variation suggests that limited sampling of single populations is unlikely to yield accurate estimates of species-wide infection rates. However, among mainland Savannah sparrows, the prevalence of malaria correlated strongly with average male size and the degree of sexual size dimorphism. We speculate that either sexual selection leads to male-biased infection or, conversely, that high rates of infection promote the evolution of strong intersexual selection.

Microsatellites reveal high levels of population substructuring in the species-poor Eretmodine cichlid lineage from Lake Tanganyika.

This study investigated fine-scale population substructuring in an apparently monogamous, biparental mouth-brooding cichlid. Microsatellite allele frequencies were determined at four polymorphic loci for nine populations of Eretmodus cyanostictus. We provide empirical support for the hypothesis that a species employing this breeding strategy should exhibit high levels of population substructuring. Stretches of sand represent considerable barriers to dispersal and, in contrast to the rock-dwelling cichlids of Lake Malawi, distance alone, along a continuous rocky shoreline, is sufficient to reduce gene flow significantly There was a significant pattern of isolation by distance both along the whole study area and over the stretch of continuous shoreline, suggesting that this species has poor dispersal capabilities and that juveniles establish territories close to their natal site. Despite limited dispersal, E. cyanostictus populations are not significantly more inbred than a more-widely dispersing rock-dwelling cichlid from Lake Malawi. This finding may cast doubt on the hypothesis that polyandry has evolved as a mechanism for maintaining genetic diversity in Lake Malawi cichlids. High levels of substructuring may not always promote high levels of speciation, and other factors, such as the intensity of sexual selection, may be more important in determining the speciation potential of a lineage.

Surprising similarity of sneaking rates and genetic mating patterns in two populations of sand goby experiencing disparate sexual selection regimes

Molecular markers have proved extremely useful in resolving mating patterns within individual populations of a number of species, but little is known about how genetic mating systems might vary geographically within a species. Here we use microsatellite markers to compare patterns of sneaked fertilization and mating success in two populations of sand goby (Pomatoschistus minutus) that differ dramatically with respect to nest-site density and the documented nature and intensity of sexual selection. At the Tvärminne site in the Baltic Sea, the microsatellite genotypes of 17 nest-tending males and mean samples of more than 50 progeny per nest indicated that approximately 35% of the nests contained eggs that had been fertilized by sneaker males. Successful nest holders mated with an average of 3.0 females, and the distribution of mate numbers for these males did not differ significantly from the Poisson expectation. These genetically deduced mating-system parameters in the Tvärminne population are remarkably similar to those in sand gobies at a distant site adjoining the North Sea. Thus, pronounced differences in the ecological setting and sexual selection regimes in these two populations have not translated into evident differences in cuckoldry rates or other monitored patterns of male mating success. In this case, the ecological setting appears not to be predictive of alternative male mating strategies, a finding of relevance to sexual selection theory.