Phillip G. Byrne

Evidence for adaptive male mate choice in the fruit fly Drosophila melanogaster.

Theory predicts that males will benefit when they bias their mating effort towards females of higher reproductive potential, and that this discrimination will increase as males become more resource limited. We conducted a series of experiments to test these predictions in a laboratory population of the fruitfly, Drosophila melanogaster. In this species, courtship and copulation have significant costs to males, and females vary greatly in fecundity, which is positively associated with body size. When given a simultaneous choice between small and large virgin females, males preferentially mated with larger, more fecund, females. Moreover, after males had recently mated they showed a stronger preference for larger females. These results suggest that male D. melanogaster adaptively allocate their mating effort in response to variation in female quality and provide some of the first support for the theoretical prediction that male stringency in mate choice increases as resources become more limiting.

Sperm competition selects for increased testes mass in Australian frogs

Game theory predicts that investment in spermatogenesis will increase with the risk and intensity of sperm competition. Widespread support for this prediction has come from comparative studies of internal fertilizing species reporting positive associations between testes mass and the probability that females mate with more than one male. Data for external fertilizers have generated conflicting results. We investigated how risk of sperm competition affects testes size in two families of Australian frogs: the Myobatrachidae and the Hylidae. We also examined effects of clutch size, egg size and oviposition location as alternative factors that might influence sperm production. Species were ranked according to probability of group spawning, and hence risk of sperm competition. Controlling for body size and phylogenetic relationships, we demonstrated that within the Myobatrachidae, the risk of sperm competition explained a significant amount of variation in testes mass. Oviposition location had a weak influence, with species ovipositing into foam having smaller testes. No significant effects of clutch size or egg size were detected. In hylids, the relationship between testes mass and risk of sperm competition was positive but not significant, again with no predictable effects related to egg size or number. These data provide an important test of sperm competition theory for externally fertilizing taxa.

Sperm competition and the evolution of gamete morphology in frogs

Despite detailed knowledge of the ultrastructure of spermatozoa, there is a paucity of information on the selective pressures that influence sperm form and function. Theoretical models for both internal and external fertilizers predict that sperm competition could favour the evolution of longer sperm. Empirical tests of the externalfertilization model have been restricted to just one group, the fishes, and these tests have proved equivocal. We investigated how sperm competition affects sperm morphology in externally fertilizing myobatrachid frogs. We also examined selection acting on egg size, and covariation between sperm and egg morphology. Species were ranked according to probability of group spawning and hence risk of sperm competition. Body size, testis size and oviposition environment may also influence gamete traits and were included in our analyses. After controlling for phylogenetic relationships between the species examined, we found that an increased risk of sperm competition was associated with increased sperm head and tail lengths. Path analysis showed that sperm competition had its greatest direct effect on sperm tail length, as might be expected under selection resulting from competitive fertilization. Sperm competition did not influence egg size. Oviposition location had a strong influence on egg size and a weak influence on sperm length, with terrestrial spawners having larger gametes than aquatic spawners. Our analysis revealed significant correlated evolution between egg morphology and sperm morphology. These data provide a conclusive demonstration that sperm competition selects for increased sperm length in frogs, and evidence for evolutionary covariance between aspects of male and female gamete morphology.

Assessing sexual conflict in the Drosophila melanogaster laboratory model system

We describe a graphical model of interlocus coevolution used to distinguish between the interlocus sexual conflict that leads to sexually antagonistic coevolution, and the intrinsic conflict over mating rate that is an integral part of traditional models of sexual selection. We next distinguish the ‘laboratory island’ approach from the study of both inbred lines and laboratory populations that are newly derived from nature, discuss why we consider it to be one of the most fitting forms of laboratory analysis to study interlocus sexual conflict, and then describe four experiments using this approach with Drosophila melanogaster. The first experiment evaluates the efficacy of the laboratory model system to study interlocus sexual conflict by comparing remating rates of females when they are, or are not, provided with a spatial refuge from persistent male courtship. The second experiment tests for a lag-load in males that is due to adaptations that have accumulated in females, which diminish male-induced harm while simultaneously interfering with a males ability to compete in the context of sexual selection. The third and fourth experiments test for a lag-load in females owing to direct costs from their interactions with males, and for the capacity for indirect benefits to compensate for these direct costs.

DOES MULTIPLE PATERNITY IMPROVE FITNESS OF THE FROG CRINIA GEORGIANA

Abstract.— In the Australian myobatrachid frog Crinia georgiana simultaneous polyandry occurs in about half of all matings, which leads to multiple paternity, but reduced fertilization success and occasional female mortality. Multiple paternity may provide benefits to females that compensate for these costs, for example, through enhanced genetic diversity of a clutch. In nature, embryos and tadpoles of C. georgiana develop in shallow, temporary pools and may be exposed to fluctuating water levels and the risk of desiccation between rain events. Fertilization by genetically diverse sires may act as a bet hedge against these conditions. To evaluate this hypothesis, females were artificially mated with one or two males in the field and eggs and larvae reared in the laboratory under constant or fluctuating developmental conditions. Experiment 1 exposed embryos from single‐ and multiple‐paternity clutches to conditions where eggs were completely covered during development or eggs sat in air on a moist substrate. Experiment 2 exposed freshly hatched larvae from single‐ and multiple‐paternity clutches to constant wet conditions, where larvae were completely covered, or fluctuating wet conditions, where larvae ranged from being completely submersed to partially exposed over a 13‐ day cycle. We measured mean performance and best performance as alternate measures of genetic benefits. There were no effects of paternity on percent survival to hatching, time to hatching, body size at hatching, percent survival to metamorphosis, time to metamorphosis, or body size at metamorphosis. We also analyzed variance within clutches as a measure of genetic diversity. Again there were no predictable effects of multiple paternity. Polyandry does not appear to provide any genetic benefits that compensate for the high costs of polyandry in this species.

Synchronous polyandry and multiple paternity in the frog Crinia georgiana (Anura: Myobatrachidae)

Multiple paternity has rarely been reported in anuran amphibians, with only three previous documented examples. For the Australian frog Crinia georgiana, we observed synchronous polyandry in an average of 44% of matings observed at four field sites. This suggests matings involving more than one male are common in this species. One to eight males were observed in amplectant groups with second males amplexed ventrally. Genetic analyses, using allozyme electrophoresis, of offspring from two matings indicated that at least two of three possible males fathered offspring. Third males were unlikely to have shared paternity, explained by their inappropriate position during amplexus. Multiple paternity may be more common in frogs than has been reported. Copyright 1999 The Association for the Study of Animal Behaviour.

Assessing the potential for an ongoing arms race within and between the sexes: selection and heritable variation

Abstract In promiscuous species, sexual selection generates two opposing male traits: offense (acquiring new mates and supplanting stored sperm) and defense (enforcing fidelity on ones mates and preventing sperm displacement when this fails). Coevolution between these traits requires both additive genetic variation and associated natural selection. Previous work with Drosophila melanogaster found autosomal genetic variation for these traits among inbred lines from a mixture of populations, but only nonheritable genetic variation was found within a single outbred population. These results do not support ongoing antagonistic coevolution between offense and defense, nor between either of these male traits and female reproductive characters. Here we use a new method (hemiclonal analysis) to study genomewide genetic variation in a large outbred laboratory population of D. melanogaster. Hemiclonal analysis estimates the additive genetic variation among random, genomewide haplotypes taken from a large, outbred, locally adapted laboratory population and determines the direction of the selection gradient on this variation. In contrast to earlier studies, we found low but biologically significant heritable variation for defensive and offensive offspring production as well as all their components (P1, fidelity, P2, and remating). Genetic correlations between these traits were substantially different from those reported for inbred lines. A positive genetic correlation was found between defense and offense, demonstrating that some shared genes influence both traits. In addition to this common variation, evidence for unique genetic variation for each trait was also found, supporting an ongoing coevolutionary arms race between defense and offense. Reproductive conflict between males can strongly influence female fitness. Correspondingly, we found genetic variation in both defense and offense that affected female fitness. No evidence was found for intersexual conflict in the context of male defense, but we found substantial intersexual conflict in the context of male offensive sperm competitive ability. These results indicate that conflict between competing males also promotes an associated arms race between the sexes.

Extreme sequential polyandry insures against nest failure in a frog

Sequential polyandry may evolve as an insurance mechanism to reduce the risk of choosing a mate that is infertile, closely related, genetically inferior or incompatible, but polyandry also might insure against nest failure in unpredictable environments. Most animals are oviparous, and in species where males provide nest sites whose quality varies substantially and unpredictably, polyandrous females might insure offspring success by distributing their eggs across multiple nests. Here, we test this hypothesis in a wild population of an Australian terrestrial toadlet, a polyandrous species, where males construct nests and remain with broods. We found that females partitioned their eggs across the nests of two to eight males and that more polyandrous females gained a significant increase in mean offspring survivorship. Our results provide evidence for the most extreme case of sequential polyandry yet discovered in a vertebrate and also suggest that insurance against nest failure might favour the evolution of polyandry. We propose that insurance against nest failure might be widespread among oviparous taxa and provide an important explanation for the prevalence of sequential polyandry in nature.

Terrestrial toadlets use chemosignals to recognize conspecifics, locate mates and strategically adjust calling behaviour

Among anuran amphibians evidence for chemical communication is scarce. We carried out three experiments to evaluate whether chemosignals influence the sexual behaviour of an Australian terrestrial toadlet, Pseudophryne bibronii. Substrate choice trials (experiment 1) revealed that females preferred to associate with substrate marked by either sex rather than an unmarked substrate and that males preferred substrate marked by females, but avoided substrate marked by other males. These results suggest that the odour of both sexes functions as a sexual attractant and that male odour may also function to repel potential male competitors. In experiment 2 we assessed whether females use male chemosignals during mate location by making gravid females navigate a two-choice Y-maze to reach calling males. Almost invariably, females followed a path outlined with male gland secretions. This result indicates that male chemosignals combined with acoustic signals improve the ability of females to find nest sites. In experiment 3 we tested whether conspecific odour influences the calling behaviour of nesting males. Female odour stimulated a twofold increase in advertisement calling and male odour stimulated a switch to territorial calling. These findings indicate that nesting males use conspecific odour as a cue for regulating investment in acoustic courtship and territory defence. Our results advance a small body of evidence to suggest that anurans use chemosignals to identify and locate potential mates and provide the first demonstration that odour can influence anuran calling behaviour.

Remating in Drosophila melanogaster: an examination of the trading-up and intrinsic male-quality hypotheses.

Female Drosophila melanogaster remate more frequently than necessary to ensure fertilization. We tested whether polyandrous females gain genetic benefits for their offspring by (1) selecting secondary sires of higher genetic‐quality than original partners or (2) because post‐copulatory mechanisms bias fertilizations towards genetically superior males. We screened 119 hemiclones of males for lifetime fitness then selected eight hemiclones (four of extreme high fitness and four of extreme low fitness) and mated them to virgin females. Females were then given the opportunity to remate with males of benchmark‐genetic quality and their propensity to remate (fidelity) and sperm displacement scored. A females fidelity and her level of sperm displacement varied depending on which hemiclone she mated first, but not on male‐genetic quality. These findings indicate that female remating and sperm displacement are strongly influenced by male genotype, but provide no evidence that these traits contribute to adaptive female choice to obtain superior genes for offspring.