MULLER'S RATCHET AND MUTATIONAL MELTDOWNS

We extend our earlier work on the role of deleterious mutations in the extinction of obligately asexual populations. First, we develop analytical models for mutation accumulation that obviate the need for time-consuming computer simulations in certain ranges of the parameter space. When the number of mutations entering the population each generation is fairly high, the number of mutations per individual and the mean time to extinction can be predicted using classical approaches in quantitative genetics. However, when the mutation rate is very low, a fixation-probability approach is quite effective. Second, we show that an intermediate selection coefficient (s) minimizes the time to extinction. The critical value of s can be quite low, and we discuss the evolutionary implications of this, showing that increased sensitivity to mutation and loss of capacity for DNA repair can be selectively advantageous in asexual organisms. Finally, we consider the consequences of the mutational meltdown for the extinction of mitochondrial lineages in sexual species.     

MUTATIONAL MELTDOWN IN LABORATORY YEAST POPULATIONS

Abstract.— In small or repeatedly bottlenecked populations, mutations are expected to accumulate by genetic drift, causing fitness declines. In mutational meltdown models, such fitness declines further reduce population size, thus accelerating additional mutation accumulation and leading to extinction. Because the rate of mutation accumulation is determined partly by the mutation rate, the risk and rate of meltdown are predicted to increase with increasing mutation rate. We established 12 replicate populations of Saccharomyces cerevisiae from each of two isogenic strains whose genomewide mutation rates differ by approximately two orders of magnitude. Each population was transferred daily by a fixed dilution that resulted in an effective population size near 250. Fitness declines that reduce growth rates were expected to reduce the numbers of cells transferred after dilution, thus reducing population size and leading to mutational meltdown. Through 175 daily transfers and approximately 2900 generations, two extinctions occurred, both in populations with elevated mutation rates. For one of these populations there is direct evidence that extinction resulted from mutational meltdown: Extinction immediately followed a major fitness decline, and it recurred consistently in replicate populations reestablished from a sample frozen after this fitness decline, but not in populations founded from a predecline sample. Wild‐type populations showed no trend to decrease in size and, on average, they increased in fitness.     

MUTATIONAL MELTDOWN IN SELFING ARABIDOPSIS LYRATA

The majority of plant species and many animals are hermaphrodites, with individuals expressing both female and male function. Although hermaphrodites can potentially reproduce by self‐fertilization, they have a high prevalence of outcrossing. The genetic advantages of outcrossing are described by two hypotheses: avoidance of inbreeding depression because selfing leads to immediate expression of recessive deleterious mutations, and release from drift load because self‐fertilization leads to long‐term accumulation of deleterious mutations due to genetic drift and, eventually, to extinction. I tested both hypotheses by experimentally crossing Arabidopsis lyrata plants (self‐pollinated, cross‐pollinated within the population, or cross‐pollinated between populations) and measuring offspring performance over 3 years. There were 18 source populations, each of which was either predominantly outcrossing, mixed mating, or predominantly selfing. Contrary to predictions, outcrossing populations had low inbreeding depression, which equaled that of selfing populations, challenging the central role of inbreeding depression in mating system shifts. However, plants from selfing populations showed the greatest increase in fitness when crossed with plants from other populations, reflecting higher drift load. The results support the hypothesis that extinction by mutational meltdown is why selfing hermaphroditic taxa are rare, despite their frequent appearance over evolutionary time.     

SPECIES RECOGNITION AND SEXUAL SELECTION AS A UNITARY PROBLEM IN ANIMAL COMMUNICATION

We investigated patterns of mating call preference and mating call recognition by examining phonotaxis of female túngara frogs, Physalaemus pustulosus, in response to conspecific and heterospecific calls. There are four results: females always prefer conspecific calls; most heterospecific calls do not elicit phonotaxis; some heterospecific calls do elicit phonotaxis and thus are effective mate recognition signals; and females prefer conspecific calls to which a component of a heterospecific call has been added to a normal conspecific call. We use these data to illustrate how concepts of species recognition and sexual selection can be understood in a unitary framework by comparing the distribution of signal traits to female preference functions.     

SEXUAL SELECTION AND THE EVOLUTION OF SEXUAL SIZE DIMORPHISM IN THE WATER STRIDER,AQUARIUS REMIGIS

Sexual size dimorphism (SSD) is often attributed to sexual selection, particularly when males are the larger sex. However, sexual selection favoring large males is common even in taxa where females are the larger sex, and is therefore not a sufficient explanation of patterns of SSD. As part of a more extensive study of the evolution of SSD in water striders (Heteroptera, Gerridae), we examine patterns of sexual selection and SSD in 12 populations of Aquarius remigis. We calculate univariate and multivariate selection gradients from samples of mating and single males, for two sexually dimorphic traits (total length and profemoral width) and two sexually monomorphic traits (mesofemoral length and wing form). The multivariate analyses reveal strong selection favoring larger males, in spite of the female-biased SSD for this trait, and weaker selection favoring aptery and reduced mesofemoral length. Selection is weakest on the most dimorphic trait, profemoral width, and is stabilizing rather than directional. The pattern of sexual selection on morphological traits is therefore not concordant with the pattern of SSD. The univariate selection gradients reveal little net selection (direct + indirect) on any of the traits, and suggest that evolution away from the plesiomorphic pattern of SSD is constrained by antagonistic patterns of selection acting on this suite of positively correlated morphological traits. We hypothesize that SSD in A. remigis is not in equilibrium, a hypothesis that is consistent with both theoretical models of the evolution of SSD and our previous studies of allometry for SSD. A negative interpopulation correlation between the intensity of sexual selection and the operational sex ratio supports the hypothesis that, as in several other water strider species, sexual selection in A. remigis occurs through generalized female reluctance rather than active female choice. The implications of this for patterns of sexual selection are discussed.     

HOMAGE TO BATEMAN: SEX ROLES PREDICT SEX DIFFERENCES IN SEXUAL SELECTION

Classic sex role theory predicts that sexual selection should be stronger in males in taxa showing conventional sex roles and stronger in females in role reversed mating systems. To test this very central prediction and to assess the utility of different measures of sexual selection, we estimated sexual selection in both sexes in four seed beetle species with divergent sex roles using a novel experimental design. We found that sexual selection was sizeable in females and the strength of sexual selection was similar in females and males in role‐reversed species. Sexual selection was overall significantly stronger in males than in females and residual selection formed a substantial component of net selection in both sexes. Furthermore, sexual selection in females was stronger in role‐reversed species compared to species with conventional sex roles. Variance‐based measures of sexual selection (the Bateman gradient and selection opportunities) were better predictors of sexual dimorphism in reproductive behavior and morphology across species compared to trait‐based measures (selection differentials). Our results highlight the importance of using assays that incorporate components of fitness manifested after mating. We suggest that the Bateman gradient is generally the most informative measure of the strength of sexual selection in comparisons across sexes and/or species.     

MODE OF SEXUAL SELECTION DETERMINED BY RESOURCE ABUNDANCE IN TWO SAND GOBY POPULATIONS

We used field observations and experiments to show that sexual selection in two populations of sand gobies, Pomatoschistus minutus (Pisces, Gobiidae), was affected by differences in resource availability. Male sand gobies rely on empty mussel shells for nest building and spawning. The two populations differed considerably in nest-site abundance and sexual-selection regimes. In one population nest sites were scarce, leading to stronger male-male competition over nests, a higher nest site colonization rate and reduced potential for female choice compared with the other population that had a surplus of nests. In the high-competition population, males were larger than females, perhaps as a response to selection, whereas the other population was not sexually size dimorphic. The results from the field were confirmed in a pool experiment that demonstrated the effect of nest abundance on nest occupancy and male reproductive success. Larger males were more successful in obtaining nest sites in both high and low nest availability treatments. Larger males were also favored by females as mating partners, but only in the treatment with surplus nest sites. Nest shortage was associated with an increased potential for intrasexual selection (measured as the coefficient of variation), whereas the potential for intersexual selection was increased when nests were common. In conclusion, nest-site abundance can influence the relative contribution of intrasexual competition and mate choice in a population. Hence, resource availability can contribute to within-species variation in mating patterns.     

TIME LAPSE ANALYSES OF SEXUAL REPRODUCTION IN CLOSTERIUM EHRENBERGII (CONJUGATOPHYCEAE)1

The process of sexual differentiation was studied using heterothallic clones of Closterium ehrenbergii Meneghini. The first visible sign of sexual reproduction was agglutination of two or more cells in a group and this was followed by gametangiogenic division and conjugation of gametangial cells. Movements of gametangial cells were carefully studied. Gametangial cells occasionally participated again in gametangiogenesis instead of proceeding directly to the formation of conjugation papilla. The whole process of sexual differentiation from vegetative cell to zygospore was considered to be basically similar in both of the two closely related mating groups, A and B, of C. ehrenbergii. Nevertheless, there were some differences between the two groups in patterns of the sexual differentiation. In Group A, vegetative cell division was completely suppressed by mixing the two complementary mating type clones together into the same medium with high light illumination. This suppression was not caused by the nitrogen depletion in the medium, but by the presence of cells of opposite mating type. In Group B, vegetative cell division and sexual reproduction occurred side by side repeatedly for several days.     

EPISTASIS,PLEIOTROPY, AND THE MUTATION LOAD IN SEXUAL AND ASEXUAL POPULATIONS

Mutation may impose a substantial load on populations, which varies according to the reproductive mode of organisms. Over the past years, various authors used adaptive landscape models to predict the long‐term effect of mutation on mean fitness; however, many of these studies assumed very weak mutation rates, so that at most one mutation segregates in the population. In this article, we derive several simple approximations (confirmed by simulations) for the mutation load at high mutation rate (U), using a general model that allows us to play with the number of selected traits (n), the degree of pleiotropy of mutations, and the shape of the fitness function (which affects the average sign and magnitude of epistasis among mutations). When mutations have strong fitness effects, the equilibrium fitness of sexuals and asexuals is close to ; under weaker mutational effects, sexuals reach a different regime where is a simple function of U and of a parameter describing the shape of the fitness function. Contrarily to weak mutation results showing that is an increasing function of population size and a decreasing function of n, these parameters may have opposite effects in sexual populations at high mutation rate.     

PURGING THE GENOME WITH SEXUAL SELECTION: REDUCING MUTATION LOAD THROUGH SELECTION ON MALES

Healthy males are likely to have higher mating success than unhealthy males because of differential expression of condition‐dependent traits such as mate searching intensity, fighting ability, display vigor, and some types of exaggerated morphological characters. We therefore expect that most new mutations that are deleterious for overall fitness may also be deleterious for male mating success. From this perspective, sexual selection is not limited to influencing those genes directly involved in exaggerated morphological traits but rather affects most, if not all, genes in the genome. If true, sexual selection can be an important force acting to reduce the frequency of deleterious mutations and, as a result, mutation load. We review the literature and find various forms of indirect evidence that sexual selection helps to eliminate deleterious mutations. However, direct evidence is scant, and there are almost no data available to address a key issue: is selection in males stronger than selection in females? In addition, the total effect of sexual selection on mutation load is complicated by possible increases in mutation rate that may be attributable to sexual selection. Finally, sexual selection affects population fitness not only through mutation load but also through sexual conflict, making it difficult to empirically measure how sexual selection affects load. Several lines of enquiry are suggested to better fill large gaps in our understanding of sexual selection and its effect on genetic load.     

MOLECULAR PHYLOGENETICS AND EVOLUTION OF SEXUAL DICHROMATISM AMONG POPULATIONS OF THE YARROW'S SPINY LIZARD (SCELOPORUS JARROVII)

Understanding evolution of geographic variation in sexually dimorphic traits is critical for understanding the role that sexual selection may play in speciation. We performed a phylogenetic analysis of geographic variation in sexual dichromatism in the Yarrow's spiny lizard (Sceloporus jarrovii), a taxon that exhibits remarkable diversity in male coloration among populations (e.g., black, red, green, yellow, blue, brown). An mtDNA phylogeny based on approximately 880 bp from the 12S ribosomal RNA gene and 890 bp from the ND4 gene was reconstructed for 30 populations of S. jarrovii and eight other species of the torquatus species group using maximum-likelihood and parsimony methods. The phylogeny suggests that S. jarrovii consists of at least five evolutionary species, none of which are sister taxa. Although intraspecific diversity in male coloration is less than indicated by previous taxonomy, two species formerly referred to as S. jarrovii exhibit impressive geographic variation in sexual dichromatism. In one of these species, the phylogeny shows the independent evolution of a distinctive blue color morph in different parts of the species range. This pattern suggests that sexual selection may lead to striking phenotypic divergence among conspecific populations and striking convergence. Results also demonstrate the importance of a phylogenetic perspective in studies of evolutionary processes within nominal species and the problematic nature of “polytypic” species recognized under the biological species concept.     

SEXUAL SELECTION IN THE BARN SWALLOW HIRUNDO RUSTICA. III. FEMALE TAIL ORNAMENTS

Male secondary sexual characters are often expressed in females, and the maintenance of the character in females can be due to either direct selection on females favoring the maintenance of the trait, or a correlated response to selection in males. Here I report on determinants of and phenotypic selection on tail length of female barn swallows Hirundo rustica. The homologous trait in males is under strong directional sexual selection. Female tail length was positively associated with several reproductive parameters including total seasonal reproductive success, even when controlling for year and age effects. A change in female tail length from one year to another was often associated with a change in the reproductive parameters correlated with absolute tail length. There was little evidence for an association between female tail length and the duration of the incubation period (only females incubate) and absolute and relative female provisioning rates of offspring, and subsequent size of offspring. Tail length of female barn swallows was positively correlated with that of their mates. Female tail length was a heritable trait as determined from regression of the tail trait of offspring on that of their mother and their father, and there was a positive genetic correlation between the tail trait in males and females. In conclusion, female tail length reliably reflects female reproductive potential, and the trait appears to be under directional selection, which may result in an evolutionary response to selection because of the heritability of the tail trait.     

REDUCED LIFESPAN AND INCREASED AGEING DRIVEN BY GENETIC DRIFT IN SMALL POPULATIONS

Explaining the strong variation in lifespan among organisms remains a major challenge in evolutionary biology. Whereas previous work has concentrated mainly on differences in selection regimes and selection pressures, we hypothesize that differences in genetic drift may explain some of this variation. We develop a model to formalize this idea and show that the strong positive relationship between lifespan and genetic diversity predicted by this model indeed exists among populations of Daphnia magna, and that ageing is accelerated in small populations. Additional results suggest that this is due to increased drift in small populations rather than adaptation to environments favoring faster life histories. First, the correlation between genetic diversity and lifespan remains significant after statistical correction for potential environmental covariates. Second, no trade‐offs are observed; rather, all investigated traits show clear signs of increased genetic load in the small populations. Third, hybrid vigor with respect to lifespan is observed in crosses between small but not between large populations. Together, these results suggest that the evolution of lifespan and ageing can be strongly affected by genetic drift, especially in small populations, and that variation in lifespan and ageing may often be nonadaptive, due to a strong contribution from mutation accumulation.     

SEXUAL CONFLICT AND INTERACTING PHENOTYPES: A QUANTITATIVE GENETIC ANALYSIS OF FECUNDITY AND COPULA DURATION IN DROSOPHILA MELANOGASTER

Many reproductive traits that have evolved under sexual conflict may be influenced by both sexes. Investigation of the genetic architecture of such traits can yield important insight into their evolution, but this entails that the heritable component of variation is estimated for males and females—as an interacting phenotype. We address the lack of research in this area through an investigation of egg production and copula duration in the fruit fly, Drosophila melanogaster. Despite egg production rate being determined by both sexes, which may cause sexual conflict, an assessment of this trait as an interacting phenotype is lacking. It is currently unclear whether copula duration is determined by males and/or females. We found significant female, but not male, genetic variance for egg production rate that may indicate reduced potential for ongoing sexually antagonistic coevolution. In contrast, copula duration was determined by significant genetic variance in both sexes. We also identified genetic variation in egg retention among virgin females. Although previously identified in wild populations, it is unclear why this should be present in a laboratory stock. This study provides a novel insight into the shared genetic architecture of reproductive traits that are the subject of sexual conflict.     

WHEN MORPHOLOGY MISLEADS: INTERPOPULATION UNIFORMITY IN SEXUAL SELECTION MASKS GENETIC DIVERGENCE IN HARLEQUIN BEETLE-RIDING PSEUDOSCORPION POPULATIONS

Differences in secondary sexual characteristics of males often provide the most conspicuous means of distinguishing between closely related species. Does this therefore imply that the absence of differentiation in exaggerated male traits between allopatric populations provides evidence of a single, genetically cohesive species? We addressed this question with a comprehensive investigation of two populations (French Guiana and Panama) of the harlequin beetle-riding pseudoscorpion, Cordylochernes scorpioides. This highly sexually dimorphic pseudoscorpion is currently described as a single species, ranging throughout the Neotropics. Our morphometric analyses detected minimal differentiation between the two populations in all nine external morphological characters measured, including sexually dimorphic traits in males. Only in traits of the spermatophore was there any appreciable level of differentiation. Behavior differentiation and prezygotic reproductive isolation were also limited: 78.3% of males successfully transferred sperm to “foreign” females, and in 63.9% of these cases, females' eggs were successfully fertilized. By contrast, extensive divergence existed in two of nine electrophoretic loci, including an essentially fixed-allele difference at the Ldh locus. Most significantly, postzygotic reproductive isolation was complete, with heteropopulation zygotes invariably aborting early in development. These results strongly suggest that the two populations are, in fact, sibling species, a conclusion supported by our recently published findings on their marked divergence in minisatellite DNA. How can such interpopulation homogeneity in male sexually dimorphic traits exist in the face of strong genetic divergence? We propose that sexual selection, oscillating between favoring small and then large males, maintains such high levels of male variability within each population that it has obscured a speciation event in which genetic divergence and postzygotic incompatibility have clearly outpaced the evolution of prezygotic reproductive isolation.     

SEXUAL DIMORPHISM,MATING SYSTEM AND BODY SIZE IN NEW WORLD BLACKBIRDS (ICTERINAE)

Although sexual selection is widely accepted as a primary functional cause of sexual size dimorphism in birds and mammals, results from some comparative studies have cast doubt on this conclusion. Chief among these contradictory results is the widespread association between body size and size dimorphism—large species tend to be more dimorphic than small species. This correlation is not directly predicted by the normal sexual selection scenario, and many hypotheses have been advanced to explain it. This paper reviews these hypotheses and evaluates them using data for the New World blackbirds (Icterinae). In this avian subfamily, (1) body size correlates with the intensity of sexual selection (as measured by mean harem size), and (2) size does not correlate with dimorphism if the effects of mating system are removed. Similar results are obtained when controlling for the confounding influence of phylogeny. Further, body size and mating system are associated with nesting dispersion. These results strongly argue that sexual dimorphism is a product of sexual selection in this subfamily, and suggest that either: (1) large body size itself, or the ecology of large species, promotes the development of coloniality and a polygynous mating system; or (2) polygyny and/or coloniality lead to the evolution of large size in both males and females. None of the other hypotheses examined predict an association between size and mating system, and all predict that size will correlate with dimorphism after the effects of mating system are removed. Thus, none of the other hypotheses seem applicable in this case. These results are compared to those obtained for other avian and mammalian taxa. Difficulties of analysis present in previous studies are discussed. I argue that it is inappropriate to assume that associations between a trait and body size or phylogeny are evidence of nonadaptive evolutionary “constraints.”     

SEXUAL SELECTION COUNTERACTS EXTINCTION OF SMALL POPULATIONS OF THE BULB MITES

Genetic drift in small populations can increase frequency of deleterious recessives and consequently lead to inbreeding depression and population extinction. On the other hand, as homozygosity at deleterious recessives increases, they should be purged from populations more effectively by selection. Sexual selection has been postulated to strengthen selection against deleterious mutations, and should thus decrease extinction rate and intensify purging of inbreeding depression. We tested these predictions in the bulb mite Rhizoglyphus robini. We created 100 replicate lines of small populations (five males and five females) and in half of them experimentally removed sexual selection by enforcing monogamy. The lines were propagated for eight generations and then assayed for purging of inbreeding depression. We found that proportion of lines which went extinct was lower with sexual selection than without. We also found evidence for purging of inbreeding depression in the lines with sexual selection, but not in lines without sexual selection. Our results suggest that purging of inbreeding depression was more effective against mutations with relatively large deleterious effects. Thus, although our data clearly indicate a positive impact of sexual selection on short‐term survival of bottlenecked populations, long‐term consequences are less clear as they may be negatively impacted by accumulation of deleterious mutations of small effect.     

SEXUAL SELECTION ON BODY SIZE AND SHAPE IN THE WESTERN HARVESTER ANT,POGONOMYRMEX OCCIDENTALIS CRESSON

Mating in social insects has generally been studied in relation to reproductive allocation and relatedness. Despite the tremendous morphological diversity in social insects, little is known about how individual morphology affects mating success. We examined the correlation of male size and shape with mating success in the western harvester ant, Pogonomyrmex occidentalis. Larger males had significantly higher mating success in two independent collections of males at mating aggregations. We also detected significant linear and nonlinear selection on aspects of male shape that were consistent across years. These shape components are independent of size, suggesting that male mating success is a complex function of size and shape. Successful males had elongate thoraxes and short mandibles relative to males collected at random at the lek. Overall, mated males also had longer postpetioles relative to body size, but there was also evidence of nonlinear selection on relative postpetiole length in both years. We found no evidence of assortative mating based on size or multivariate shape measures in either year, but in one year we found weak assortative mating based on some univariate traits.