Alternative reproductive tactics in male freshwater fish influence the accuracy of species recognition

Sexual conflict can result in coercive mating. Because males bear low costs of heterospecific mating, coercive males may engage in misdirected mating attempts toward heterospecific females. In contrast, sexual selection through consensual mate choice can cause mate recognition cues among species to diverge, leading to more accurate species recognition. Some species show both coercive mating and mate choice‐associated courtship behaviors as male alternative reproductive tactics. We hypothesized that if the selection pressures on each tactic differ, then the accuracy of species recognition would also change depending on the mating tactic adopted. We tested this hypothesis in the guppy (Poecilia reticulata) and mosquitofish (Gambusia affinis) by a series of choice experiments. Poecilia reticulata and G. affinis males both showed imperfect species recognition and directed all components of mating behavior toward heterospecific females. They tended to direct courtship displays more frequently toward conspecific than heterospecific females. With male P. reticulata, however, accurate species recognition disappeared when they attempted coercive copulation: they directed coercions more frequently toward heterospecific females. We also found that heterospecific sexual interaction had little effect on the fecundity of gravid females, which suggests that prepregnancy interactions likely underpin the exclusion of G. affinis by P. reticulata in our region.     

Selection by Fertility in DROSOPHILA PSEUDOOBSCURA

Fertility, the component of selection due to female fecundity and male mating success, differed significantly among the ST/ST, ST/AR, and AR/AR karyotypes in experimental populations and varied with karyotypic frequency. In relation to ST/AR, ST/ST females and males had higher fertilities at low frequency; AR/AR males and females were at a significant fertility disadvantage at intermediate frequency, while at low and at high frequencies their fertilities matched or exceeded that of the heterokaryotype. These fertility differences were comparable in size to viability differences previously reported for D. pseudoobscura karyotypes. Differential fertility seems likely to be an important element, perhaps just as important as differential viability, in the balancing selection that maintains the chromosomal polymorphism in this species.     

Esterase-6 polymorphism inDrosophila melanogaster:Effects of temperature and methyl malonate on genotypic trajectories in polymorphic populations set up with highly inbred lines

It is generally difficult to identify possible effects of selection at a specific locus because of the heterogeneity of the genetic background. Geographical patterns ofEst-6 gene frequencies suggest that there is selection at this locus but selection on loci closely linked to it cannot be excluded. Differences in catalytic properties between allozymes have been shownin vitro; further, several laboratory studies have shown apparent fitness differences between allozymes. Our study used inbred lines highly homogeneous in the genetic background. Four populations were set up fromEst-6s andEst-6F homozygous females inseminated by males of the same genotype at each combination of three factors: temperature (18 and 25°C); methyl malonate (presence or absence); input gene frequencies [p(S) = 0.2 and 0.8]. The populations were sampled periodically for about 28 generations. Methyl malonate was chosen to exert pressure in the enzymatic function of esterase-6. Statistical analyses show that: there are no sex differences; gene frequencies change from input values to those of the first sampling, when only individuals of the first generation are present at 18^oC or individuals of the second generation just begin to appear at 25°C; gene frequencies do not change thereafter and Hardy-Weinberg equilibrium is established. The changes in gene frequencies observed in the first generations suggest thatEst-6 can under certain conditions be a target of selection. Such conditions may not, however, occur in natural populations.     

Loss of cytoplasmic incompatibility and minimal fecundity effects explain relatively low Wolbachia frequencies in Drosophila mauritiana

Maternally transmitted Wolbachia bacteria infect about half of all insect species. Many Wolbachia cause cytoplasmic incompatibility (CI) and reduced egg hatch when uninfected females mate with infected males. Although CI produces a frequency‐dependent fitness advantage that leads to high equilibrium Wolbachia frequencies, it does not aid Wolbachia spread from low frequencies. Indeed, the fitness advantages that produce initial Wolbachia spread and maintain non‐CI Wolbachia remain elusive. wMau Wolbachia infecting Drosophila mauritiana do not cause CI, despite being very similar to CI‐causing wNo from Drosophila simulans (0.068% sequence divergence over 682,494 bp), suggesting recent CI loss. Using draft wMau genomes, we identify a deletion in a CI‐associated gene, consistent with theory predicting that selection within host lineages does not act to increase or maintain CI. In the laboratory, wMau shows near‐perfect maternal transmission; but we find no significant effect on host fecundity, in contrast to published data. Intermediate wMau frequencies on the island of Mauritius are consistent with a balance between unidentified small, positive fitness effects and imperfect maternal transmission. Our phylogenomic analyses suggest that group‐B Wolbachia, including wMau and wPip, diverged from group‐A Wolbachia, such as wMel and wRi, 6–46 million years ago, more recently than previously estimated.     

The genetic mating structure of subdivided populations I. Open-mating model

The genetic mating structure of a subdivided population can describe how parental genotypes gave rise to zygotes. When parents of the same genotype are considered together as one class (“open-mating”), three independent parameters of inbreeding and mating structure are needed to describe this structure at a diallelic locus. One is Wright's fixation index F. The other two are mating structure parameters, derived herein and termed the “effective selfing” rate E and the “inbreeding assortative selfing” rate D. E is the genetically equivalent proportion of self-fertilization at a single locus, and is given by standardized second and third central moments of gene frequencies of mates. E is a summary measure of inbreeding that includes effects due to self-fertilization and mating to relatives, as well as correlations between mates induced by Wahlund effects and/or selective diversification among neighborhoods. The second parameter D measures the tendency of inbred or more homozygous individuals to effectively self more (or less) than outbred or more heterozygous individuals. D is related to the maintenance of variation of inbreeding among individuals and/or to the prevalence of spatial variation of selection. D is independent of E, but together with E controls the generational change of inbreeding, ΔF. Extensions of the model to unequal allele frequencies in male vs female mates, and to multi-allelic loci, are also examined.     

Fitness of Allozyme Variants in DROSOPHILA PSEUDOOBSCURA. I. Selection at the PGM-1 and ME-2 Loci

We have studied in Drosophila pseudoobscura the effect of allozyme variation on seven fitness components: female fecundity, egg hatchability, egg-to-adult survival under near-optimal and under competitive conditions, rate of development under near-optimal and under competitive conditions, and mating capacity of males. Three genotypes at each of two loci, Pgm-1 and Me-2, have been studied in various combinations. These two loci are highly polymorphic in natural populations of D. pseudoobscura. Statistically significant differences involving one or more genotypes exist for all components of fitness. No single genotype is best for all fitness components; rather the relative fitnesses of genotypes are reversed when different parameters are considered, or when they are studied in different environmental conditions. Also, the average egg-to-adult survival and rate of development are better when different genotypes are reared together than when they occur in pure culture. Four different modes of selection have been uncovered by our experiments. These forms of selection may account for the persistence of the two allozyme polymorphisms in nature, and for previously observed seasonal fluctuations of the allelic frequencies in natural populations.     

Number of mating males and mating interval affect last-male sperm precedence in Tenebrio molitor L.

Polyandrous females often mate with more than two males, and yet most studies of postcopulatory sexual selection involve only two males. In insects, second-male sperm precedence is usually taken as evidence of overall last-male sperm precedence despite some studies to the contrary. Furthermore, the processes or mechanisms causing the patterns are often unknown and yet are important when estimating how postcopulatory sexual selection might act on males. Whether the patterns and processes change in normal sperm competitive situations and the effects of other factors besides mating order need to be examined to better assess the evolutionary potential of postcopulatory sexual selection. In this study, I assessed the effects of mating interval and number of mating males on sperm precedence patterns and their causal mechanisms in the mealworm beetle, Tenebrio molitor. Last-male sperm precedence was the same when two or three males mated, but also depended on mating intervals and hence mechanisms of paternity bias. However, when females mated with many males, one of the mechanisms no longer created last-male sperm precedence. This example illustrates the importance of knowing both the patterns and mechanisms of paternity bias and whether they change depending on female mating frequency to make reasonable inferences about the potential for postcopulatory sexual selection on males. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.      

Evolutionary causes of male-biased sexual size dimorphism from a female perspective in the seed bug Togo hemipterus (Heteroptera: Lygaeidae)

Sexual size dimorphisms (SSDs) in body size are expected to evolve when selection on female and male sizes favors different optima. Many insects show female-biased SSD that is usually explained by the strong fecundity advantage of larger females. However, in some insects, males are as large as or even larger than females. The seed bug Togo hemipterus (Scott) also exhibits a male-biased SSD in body size. Many studies that have clarified the evolutionary causes of male-biased SSD have focused only on male advantages due to male–male competition. To clarify the evolutionary causes of male-biased SSD in body size, we should examine the degree of not only the sexual selection that favors larger males but also natural selection that is acting on female fecundity. The obtained results, which showed higher mating acceptance rates to larger males, implies that females prefer larger males. No significant relationship was detected between female body size and fecundity; body size effects on female fecundity were weak or undetectable. We conclude that male-biased SSD in T. hemipterus can be accounted for by a combination of sexual selection through male–male competition and female choice favoring large males, plus weak or undetectable natural selection that favors large females due to a fecundity advantage.     

Wolbachia-Based Population Control Strategy Targeting Culex quinquefasciatus Mosquitoes Proves Efficient under Semi-Field Conditions

In mosquitoes, the maternally inherited bacterial Wolbachia induce a form of embryonic lethality called cytoplasmic incompatibility (CI). This property can be used to reduce the density of mosquito field populations through inundative releases of incompatible males in order to sterilize females (Incompatible Insect Technique, or IIT, strategy). We have previously constructed the LR[wPip(Is)] line representing a good candidate for controlling field populations of the Culex quinquefasciatus mosquito in the islands of the south-western Indian Ocean. The main purpose of the present study was to fill the gap between laboratory experiments and field implementation, i.e. assessing mating competitiveness of these incompatible males under semi-field conditions. In a first set of experiments, we analyzed crossing relationships between LR[wPip(Is)] males and La Réunion field females collected as larvae in 19 distinct localities throughout the island. This investigation revealed total embryonic mortality, confirming the strong sterilizing capacity of LR[wPip(Is)] males. Subsequently, mating competitiveness of LR[wPip(Is)] males was assessed under semi-field conditions in the presence of field males and females from La Réunion. Confrontations were carried out in April and December using different ratios of LR[wPip(Is)] to field males. The results indicated that the LR[wPip(Is)] males successfully compete with field males in mating with field females, displaying even higher competitiveness than field males in April. Our results support the implementation of small-scale field tests in order to assess the feasibility of IIT against Cx. quinquefasciatus in the islands of southwestern Indian Ocean where this mosquito species is a proven competent vector for human pathogens.     

A re-examination of Wolbachia-induced cytoplasmic incompatibility in California Drosophila simulans

Background

In California Drosophila simulans, the maternally inherited Riverside strain Wolbachia infection (wRi) provides a paradigm for rapid spread of Wolbachia in nature and rapid evolutionary change. wRi induces cytoplasmic incompatibility (CI), where crosses between infected males and uninfected females produce reduced egg-hatch. The three parameters governing wRi infection-frequency dynamics quantify: the fidelity of maternal transmission, the level of cytoplasmic incompatibility, and the relative fecundity of infected females. We last estimated these parameters in nature in 1993. Here we provide new estimates, under both field and laboratory conditions. Five years ago, we found that wRi had apparently evolved over 15 years to enhance the fecundity of infected females; here we examine whether CI intensity has also evolved.

Methodology/Principal Findings

New estimates using wild-caught flies indicate that the three key parameters have remained relatively stable since the early 1990s. As predicted by our three-parameter model using field-estimated parameter values, population infection frequencies remain about 93%. Despite this relative stability, laboratory data based on reciprocal crosses and introgression suggest that wRi may have evolved to produce less intense CI (i.e., higher egg hatch from incompatible crosses). In contrast, we find no evidence that D. simulans has evolved to lower the susceptibility of uninfected females to CI.

Conclusions/Significance

Evolution of wRi that reduces CI is consistent with counterintuitive theoretical predictions that within-population selection on CI-causing Wolbachia does not act to increase CI. Within taxa, CI is likely to evolve mainly via pleiotropic effects associated with the primary targets of selection on Wolbachia, i.e., host fecundity and transmission fidelity. Despite continuous, strong selection, D. simulans has not evolved appreciably to suppress CI. Our data demonstrate a lack of standing genetic variation for CI resistance in the host.     

Frequency-Dependent Selection at the LAP Locus in DROSOPHILA MELANOGASTER

Results of fitness estimates for the Lap locus in Drosophila melanogaster revealed that under crowded media conditions gene frequency equilibrium was maintained by frequency-dependent selection. Evidence was obtained that indicated that mating and egg-to-adult viability were frequency dependent.     

Rapid Sequential Spread of Two Wolbachia Variants in Drosophila simulans

The maternally inherited intracellular bacteria Wolbachia can manipulate host reproduction in various ways that foster frequency increases within and among host populations. Manipulations involving cytoplasmic incompatibility (CI), where matings between infected males and uninfected females produce non-viable embryos, are common in arthropods and produce a reproductive advantage for infected females. CI was associated with the spread of Wolbachia variant wRi in Californian populations of Drosophila simulans, which was interpreted as a bistable wave, in which local infection frequencies tend to increase only once the infection becomes sufficiently common to offset imperfect maternal transmission and infection costs. However, maternally inherited Wolbachia are expected to evolve towards mutualism, and they are known to increase host fitness by protecting against infectious microbes or increasing fecundity. We describe the sequential spread over approximately 20 years in natural populations of D. simulans on the east coast of Australia of two Wolbachia variants (wAu and wRi), only one of which causes significant CI, with wRi displacing wAu since 2004. Wolbachia and mtDNA frequency data and analyses suggest that these dynamics, as well as the earlier spread in California, are best understood as Fisherian waves of favourable variants, in which local spread tends to occur from arbitrarily low frequencies. We discuss implications for Wolbachia-host dynamics and coevolution and for applications of Wolbachia to disease control.     

THE EVOLUTIONARY HISTORY OF DROSOPHILA BUZZATII. VIII. EVIDENCE FOR ENDOCYCLIC SELECTION ACTING ON THE INVERSION POLYMORPHISM IN A NATURAL POPULATION

The pattern of selection acting in nature on the chromosomal polymorphism of the cactophilic species Drosophila buzzatii was investigated by comparing inversion and karyotypic frequencies through four different life-cycle stages: adult males, eggs, third-instar larvae, and immature adults. All population samples were obtained in June 1981 at an old Opuntia ficus-indica plantation near Carboneras, Spain. The analysis rests on several assumptions which are explicitly set forth and discussed. The results, if these assumptions prove true, indicate strong directional selection for larval viability acting on the second-chromosome karyotypes and also suggest selective differences in fecundity and longevity. Heterotic selection, however, cannot be ruled out for other fitness components such as male mating success. This kind of selection could be operating on the fourth-chromosome polymorphism as well. Some gene arrangements showed significant and opposite changes in frequency at different parts of the life cycle, thus demonstrating endocyclic selection.     

Activity Variants of Acid Phosphatase-3 among Chromosome 3 Inversions of DROSOPHILA PSEUDOOBSCURA

Sexual selection is measured between two strains of Drosophila melanogaster: a wild strain and a strain mutant at the sepia locus. Frequency-dependent male mating was found to be successful, whereas the female genotype exerted no influence. The rarer the male genotype becomes, the greater is its mating success. A selection model is built for this behavior characteristic in which selection operates differently in the two sexes. The genetic consequencies of this model upon the maintenance of genetic polymorphism at the sepia locus are compared to experimental data from previous population cage studies. The fit obtained with this sexual selection model is compared to that of the larvel selection model previously investigated. A model composed of both sexual and larval components of fitness is presented. The role that each major selection component is expected to play in experimental populations as the gene frequency changes is discussed. Sexual selection leads to an equilibrium level higher than larval selection, and the combined model is very close to the experimental values.     

Mate choice for non-additive genetic benefits: a resolution to the lek paradox

In promiscuous mating systems, females often show a consistent preference to mate with one or a few males, presumably to acquire heritable genetic benefits for their offspring. However, strong directional selection should deplete additive genetic variation in fitness and consequently any benefit to expressing the preference by females (referred to as the lek paradox). Here, we provide a novel resolution that examines non-additive genetic benefits, such as overdominance or inbreeding, as a source of genetic variation. Focusing on the inbreeding coefficient f and overdominance effects, we use dynamic models to show that (1) f can be inherited from sire to offspring, (2) populations with females that express a mating preferences for outbred males (low f) maintain higher genetic variation than populations with females that mate randomly, and (3) preference alleles for outbred males can invade populations even when the alleles are associated with a fecundity cost. We show that non-additive genetic variation due to overdominance can be converted to additive genetic variation and becomes “heritable” when the frequencies of alternative homozygous genotypes at fitness loci deviate from equality. Unlike previous models that assume an infinite population size, we now show that genetic drift in finite populations can lead to the necessary deviations in the frequencies of homozygous genotypes. We also show that the “heritability of f,” and hence the benefit to a mating preference for non-additive genetic benefits, is highest in small populations and populations in which a smaller number of loci contribute to fitness via overdominance. Our model contributes to the solution of the lek paradox.     

Does heterospecific seminal fluid reduce fecundity in interspecific copulation between seed beetles?

Reproductive interference through mating between related species can cause fitness reduction and affect population dynamics of the interacting species. In experimental matings between two seed beetles, Callosobruchus chinensis and Callosobruchus maculatus, C. maculatus females, but not C. chinensis females, suffer from significant loss of fecundity when conspecific mating is followed by heterospecific mating. We hypothesized that male traits associated with sexual conflict, which are often harmful to females, pleiotropically affect fitness of heterospecific females through interspecific mating. We examined the effect of ejaculate of C. chinensis males on C. maculatus females as the cause of the fecundity loss in C. maculatus females due to interspecific copulation. We found that frequent interspecific copulation occurred between C. maculatus females and C. chinensis males, but not between C. chinensis females and C. maculatus males, resulting in frequent interspecific ejaculate transfer from C. chinensis males to C. maculatus females. However, injection of the extract from C. chinensis male reproductive organs into C. maculatus females did not significantly affect C. maculatus fecundity compared with saline injection, indicating that the effect of the heterospecific ejaculate transfer on fecundity is negligible. We suggest that other harmful male traits such as genital spines of C. chinensis males are mainly responsible for the fecundity reduction in C. maculatus females that have experienced interspecific mating.     

Antagonistic selection factors induce a continuous population divergence in a polymorphism

Understanding the relative importance of selection and stochastic factors in population divergence of adaptive traits is a classical topic in evolutionary biology. However, it is difficult to separate these factors and detect the effects of selection when two or more contrasting selective factors are simultaneously acting on a single locus. In the damselfly Ischnura senegalensis, females exhibit color dimorphism and morph frequencies change geographically. We here evaluated the role of selection and stochastic factors in population divergence of morph frequencies by comparing the divergences in color locus and neutral loci. Comparisons between population pairwise F_ST for neutral loci and for the color locus did not detect any stochastic factors affecting color locus. Although comparison between population divergence in color and neutral loci using all populations detected only divergent selection, we detected two antagonistic selective factors acting on the color locus, that is, balancing and divergent selection, when considering geographical distance between populations. Our results suggest that a combination of two antagonistic selective factors, rather than stochastic factors, establishes the geographic cline in morph frequency in this system.     

Evolution of female colour polymorphism in damselflies: testing the hypotheses

The existence of several female colour morphs is a conspicuous characteristic of many damselflies that show one male-like (androchrome) and several nonmale-like (gynochrome) morphs. We tested several adaptive hypotheses and the null model for the maintenance of female polychromatism (one androchrome and two gynochromes) in the damselfly Ceriagrion tenellum. We tested the null model by comparing the degree of genetic differentiation between the colour locus and a set of 19 neutral RAPD loci in five populations. Our results indicate that selection is acting to maintain similar frequencies between populations at the colour locus. Using mark–recapture techniques we found that mating success is not dependent on female coloration. We tested the mimicry hypothesis by presenting live and dead models to males. Dead models were highly attractive irrespective of coloration. In contrast, with live models males could not distinguish between androchromes and other males, and were more attracted to gynochrome females. Despite this, within populations morph frequencies remained constant over time and mating was at random with respect to female coloration. However, there was a positive relationship between male density and androchrome frequency in a comparative study of eight populations. We discuss our results in the framework of sexual conflict theory and suggest that andro- and gynochrome females are using different strategies to control their number of matings. The different morphs might be maintained in a balanced polymorphism by a combination of density- and frequency-dependent mechanisms.Copyright 2002 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour     

The role of mating history and male size in determining mating behaviours and sexual conflict in a water strider

We conducted three experiments to test the effects of mating history of both sexes and of male body size on mating behaviours in the water strider, Gerris buenoi. Our manipulations influenced the interests of both sexes and, thus, the degree of conflict over mating behaviours. Mating history was a dichotomous variable (deprived/mated), depending on holding conditions in the laboratory. Experiment 1 considered and found independent effects of male and female mating history on latency to copulation and copulation duration. In experiment 2, we manipulated only female mating history, using unsuccessful struggle rates as evidence for female reluctance and conflict over mating. Finally, we investigated the relation between male body size and mating history on copulation duration. We predicted that intersexual conflict over mating would be lowest when females were deprived, because female interests under these conditions should more closely match those of males. Deprived females began mating in half the time of mated females and were twice as likely to mate because of reduced reluctance. Furthermore, copulation duration for deprived males was about one and a half times longer than that for mated males. Although previous studies examining nonrandom mating patterns by size predicted longer copulations for small males, we found that small males prolonged copulation when deprived more than large males. We conclude that females primarily influence copulation frequency, but males primarily influence copulation duration. Our results favour the hypothesis that reduced mating opportunity for small males accounts for their extended copulation duration. Finally, our findings provide evidence for strong effects of male body size on selection mechanisms in water striders, and support the hypothesis of conflicting pre- and postcopulatory selection mechanisms in this group. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.     

Selection at the Esterase-2 Locus of Drosophila buzzatii? Perturbation-Reperturbation Experiments

Apparent selection affecting starch gel electrophoretic alleles at the Esterase-2 locus of Drosophila buzzatii has been detected in laboratory and natural populations. Perturbation-reperturbation of allele frequencies in replicated laboratory populations attempts to test direct selective effects at the locus versus effects of linked loci. Sequential gel electrophoresis has identified more alleles within starch classes, and three of these alleles (within the a, b and c starch alleles) were used in cage population experiments. Allele a/1.00/1.00/1.00 was set up in 10 replicate populations with allele c/1.00/1.00/1.00, and in an independent 10 replicate populations with allele b/0.99/1.01/1.00. For each set, three reperturbations were done. Replicate populations generally showed similar patterns of allele frequency change and clear directionality: effects of selection, not drift. However, four populations deviated from their replicates, indicating dissipation of linkage disequilibrium. Estimates of pre-adult viability in the F₂ of pair-wise crosses among 12 sequential gel electrophoretic alleles showed very variable modes of inheritance and relative viability fitnesses. Together with the diversity of patterns of allele frequency change in the cage populations, these results suggest a gene complex, with selection acting on an interacting set of loci which may include Esterase-2.