Mating frequency of ant queens with alternative dispersal strategies, as revealed by microsatellite analysis of sperm

In social Hymenoptera (ants, bees, and wasps), the number of males that mate with the same queen affects social and genetic organization of the colony. However, the selective forces leading to single mating in certain conditions and multiple mating in others remain enigmatic. In this study, I investigated whether queens of the wood ant Formica paralugubris adopting different dispersal strategies varied in their mating frequency (the number of males with whom they mated). The frequency of multiple mating was determined by using microsatellite markers to genotype the sperm stored in the spermatheca of queens, and the validity of this method was confirmed by analysing mother–offspring combinations obtained from experimental single-queen colonies. Dispersing queens, which may found new colonies, did not mate with more males than queens that stayed within polygynous colonies, where the presence of numerous reproductive individuals ensured a high level of genetic diversity. Hence, this study provides no support to the hypotheses that multiple mating is beneficial because it increases genetic variability within colonies. Most of the F. paralugubris queens mated with a single male, whatever their dispersal strategy and life history. Moreover, multiple mating had little effect on colony genetic structure: the effective mating frequency was 1.11 when calculated from within-brood relatedness, and 1.13 when calculated from the number of mates detected in the sperm. Hence, occasional multiple mating by F. paralugubris queens may have no adaptive significance.     

Strict monandry in the ponerine army ant genus Simopelta suggests that colony size and complexity drive mating system evolution in social insects

Altruism in social insects has evolved between closely related full-siblings. It is therefore of considerable interest why some groups have secondarily evolved low within-colony relatedness, which in turn affects the relatedness incentives of within-colony cooperation and conflict. The highest queen mating frequencies, and therefore among the lowest degrees of colony relatedness, occur in Apis honeybees and army ants of the subfamilies Aenictinae, Ecitoninae, and Dorylinae, suggesting that common life history features such as reproduction by colony fission and male biased numerical sex-ratios have convergently shaped these mating systems. Here we show that ponerine army ants of the genus Simopelta, which are distantly related but similar in general biology to other army ants, have strictly monandrous queens. Preliminary data suggest that workers reproduce in queenright colonies, which is in sharp contrast to other army ants. We hypothesize that differences in mature colony size and social complexity may explain these striking discrepancies.     

Polygyny and polyandry in small ant societies

Social insects, ants in particular, show considerable variation in queen number and mating frequency resulting in a wide range of social structures. The dynamics of reproductive conflicts in insect societies are directly connected to the colony kin structure, thus, the study of relatedness patterns is essential in order to understand the evolutionary resolution of these conflicts. We studied colony kin structure and mating frequencies in two closely related Neotropical ant species Pachycondyla inversa and Pachycondyla villosa. These represent interesting model systems because queens found new colonies cooperatively but, unlike many other ant species, they may still co-exist when the colony becomes mature (primary polygyny). By using five specific and highly variable microsatellite markers, we show that in both species queens usually mate with two or more males and that cofounding queens are always unrelated. Polygynous and polyandrous colonies are characterized by a high genetic diversity, with a mean relatedness coefficient among worker nestmates of 0.27 (+/- 0.03 SE) for P. inversa and 0.31 (+/- 0.05 SE) for P. villosa. However, relatedness among workers of the same matriline is high (0.60 +/- 0.03 in P. inversa, 0.62 +/- 0.08 in P. villosa) since males that mated with the same queen are on average closely related. Hence, we have found a new taxon in social Hymenoptera with high queen-mating frequencies and with intriguing mating and dispersal patterns of the sexuals.     

Asynchronous arrival pattern, operational sex ratio and occurrence of multiple paternities in a territorial breeding anuran, Rana dalmatina

Understanding why females mate multiply is a major issue in evolutionary ecology. We investigated the consequences of an asynchronous arrival pattern on male competition and multiple paternity in the apparently monoandrous agile frog ( Rana dalmatina ). The largest frogs arrived first and both males and females lost weight significantly during the spawning period. Asynchronous arrival at breeding sites resulted in a male-biased operational sex ratio (OSR). The OSR was more strongly male-biased at the beginning and at the end of the breeding period when the number of satellite males increased. All females mated only once, but multiple paternity within clutches occurred at the beginning and the end of the breeding period. The influence of asynchronous arrival and biased sex ratio suggests that reduced variance or bet-hedging promoting female fitness had only a reduced role in the evolution of polyandry, and polyandry is likely to be associated with male benefits. Polyandry in frogs can be explained either by forced mating as a result of sexual conflict or by clutch piracy. By modifying intrasexual competition, asynchronous arrival and changes in OSR may have a decisive influence upon the evolution of mating systems and favour both polyandry and stable coexistence of alternative mating behaviour.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 86 , 191–200.     

The economics of brood raiding and nest consolidation during ant colony founding

Summary The most dangerous time for an ant colony is during the founding stage when the small colony is vulnerable to predation and competition. Colonies can grow more rapidly when multiple queens cooperate in raising the first worker brood (pleometrosis) or by raiding other incipient colonies for their brood. This brood raiding has been proposed to be the primary force selecting for pleometrosis, i.e. multiple-queen colonies may have a considerable advantage in destroying neighbours by aggressively stealing their brood. An alternative hypothesis is that incipient nests are part of a larger, interconnected population structure and that brood raiding reflects cooperative pleometrosis with subdivided colonies. A simple mathematical model supports the second hypothesis: workers of incipient colonies are especially favoured to peaceably abandon their nest and join with other colonies if the queens are related or queens from raided colonies can infiltrate the raiding colony. The latter condition is often met in ant species that brood raid and particularly exemplified in fire ants (Solenopsis invicta), where brood raiding involves little mortal combat and combines with pleometrosis to rapidly increase colony size. It is proposed that the term nest consolidation should replace brood raiding to more accurately reflect the relatively non-aggressive and potentially apparently cooperative nature of interactions between incipient ant colonies.     

The frequency of multiple paternity predicts variation in testes size among island populations of house mice

Polyandry generates selection on males through sperm competition, which has broad implications for the evolution of ejaculates and male reproductive anatomy. Comparative analyses across species and competitive mating trials within species have suggested that sperm competition can influence the evolution of testes size, sperm production and sperm form and function. Surprisingly, the intraspecific approach of comparing among population variation for investigating the selective potential of sperm competition has rarely been explored. We sampled seven island populations of house mice and determined the frequency of multiple paternity within each population. Applying the frequency of multiple paternity as an index of the risk of sperm competition, we looked for selective responses in male reproductive traits. We found that the risk of sperm competition predicted testes size across the seven island populations of house mice. However, variation in sperm traits was not explained by sperm competition risk. We discuss these findings in relation to sperm competition theory, and other intrinsic and extrinsic factors that might influence ejaculate quality.     

Multiple paternity in wild-caught Drosophila mojavensis

Female remating frequency and sperm allocation patterns can strongly influence levels of sperm competition and reproductive success in natural populations. In the laboratory, Drosophila mojavensis males transfer very few sperm per copulation and females remate often, suggesting multiple paternity should be common in nature. Here, we examine female sperm loads, incidence of multiple paternity, and sperm utilization by genotyping progeny from 20 wild-caught females at four highly polymorphic microsatellite loci. Based on indirect paternity analyses of 814 flies, we found evidence for high levels of multiple paternity coupled with relatively low reproductive output, consistent with the high levels of female remating predicted in this sperm-limited species. Overall, we found little evidence for last -- male sperm precedence though some temporal variation in sperm utilization was observed, consistent with laboratory findings.     

Polyandry in the wild: temporal changes in female mating frequency and sperm competition intensity in natural populations of the tettigoniid Requena verticalis

Empirical tests of sexual selection theory generally utilize model systems under laboratory settings, and extend conclusions to evolutionary processes occurring in nature. The biological significance of laboratory findings will depend largely on the mating rates of females and patterns of paternity in natural populations, information on which is generally lacking. Here we use microsatellite markers to provide rare estimates of female mating rates and patterns of parentage in a species of tettigoniid, Requena verticalis, which has been used extensively to test theory on the evolution of male parental investment and its influence on the direction of sexual selection. We found that although the number of males having a genetic representation in the female's sperm stores was higher for females collected late in the breeding season than those collected early in the season, overall the female mating rate was lower than that expected from laboratory observations. Analysis of parentage of offspring produced by females at the end of the breeding season revealed that all males represented in the sperm stores fathered offspring, although paternity was biased away from that expected from random sperm utilization. The data show that the complete first male sperm precedence documented in laboratory studies of this species does not persist in natural populations. Our data provide a solid underpinning for conclusions drawn from laboratory studies of this species.     

A genetic component in the determination of worker polymorphism in the Florida harvester ant Pogonomyrmex badius

Summary. The interplay of genetic and environmental factors in the determination of social insect castes has long intrigued biologists. Though an overwhelming majority of studies establish that factors such as nutrition, pheromones and temperature determine the developmental fate of worker larvae, genetic components have recently been shown to play a role in the determination of morphological worker castes in leaf-cutting ants. Here we demonstrate that the determination of worker castes in the strongly polyandrous Florida harvester ant, Pogonomyrmex badius, has a genetic component. The overall distribution of caste members among patrilines in our study colonies is significantly different from the intracolonial caste ratio. Though this effect was not apparent in all colonies, our results suggest that workers of different patrilines in P. badius differ significantly in their propensities to develop into a certain worker caste. This genetic basis of worker polymorphism may go unnoticed in many social hymenopterans because of their low intracolonial genetic diversity due to monogamous colony structure. The worker polymorphism of P. badius is a taxonomic isolate and presumably a young trait in the genus. Therefore, a common genetic component of the determination of morphological and behavioral worker castes in social insects might be farranging taxonomically and may even be based on a genetic machinery inherent to all hymenopterans, but dormant in most.Received 3 May 2004; revised 27 October 2004; accepted 8 November 2004.