David J. Hosken

Sperm competition in bats

Sperm competition is a widespread phenomenon influencing the evolution of male anatomy, physiology and behaviour. Bats are an ideal group for studying sperm competition. Females store fertile sperm for up to 200 days and the size of social groups varies from single animals to groups of hundreds of thousands. This study examines the relationship between social group size and investment in spermatogenesis across 31 species of microchiropteran bat using new and published data on testis mass and sperm length. In addition to male competition, I examined the effects of female reproductive biology on characteristics of spermatogenesis. Comparative studies indicate that relative testis mass is positively related to sperm competition risk in a wide range of taxa. Social group size may also influence the level of sperm competition, and one of the costs of living in groups may be decreased confidence of paternity. I used comparative analysis of independent contrast (CAIC) to control for phylogeny. Using two possible phylogenies and two measures of social group size, I found a significant positive relationship between social group size and testis mass. There was no relationship between testis mass and the dimension of the female reproductive tract or oestrus duration. Sperm length was not significantly related to body mass or group size, nor was it related to oestrus duration.

The evolution of reproductive isolation through sexual conflict.

Classical population-genetics theory suggests that reproductive isolation will evolve fastest in small isolated populations. In contrast, recent theory suggests that divergence should occur fastest in larger allopatric populations. The rationale behind this is that sexual conflict, potentially the strongest driver of speciation, is greater in larger, higher-density populations. This idea is highly controversial and has little experimental support. Here we show, using replicate fly populations with varying levels of sexual conflict, that larger, more dense populations with more sexual conflict diverged to a greater degree than small populations with relaxed conflict. This result strongly suggests that speciation can occur rapidly in large populations through increased sexual conflict.

Sperm morphological diversity

Publisher Summary This chapter reviews the current knowledge of variation in sperm morphology over several levels of biological organization: variation within males (both within and across ejaculates), among males, among populations, and among species, along with prevailing hypotheses addressing the adaptive significance of such variation. With regard to developmental mechanisms, three aspects of the physiology of sperm production serve to limit within-ejaculate variation in sperm phenotypes. First, the location of the testes and numerous aspects of testicular physiology of some taxa are clearly adaptations to maintain a homeostatic developmental environment for sperm. Second, developing spermatids may share cytoplasm. Third, sperm phenotypes are predominantly determined by testicular gene expression and hence the diploid genome of the male. Variation across ejaculates but within males can involve several traits including sperm numbers, overall semen quality and individual sperm quality. A special case of intramale variation in sperm form is found in species with sperm heteromorphism, in which different sperm forms are regularly produced by individuals. Differences among males in sperm morphology may derive from both genetic and environmental influences. Theories of condition-dependence basically posit that fitness-related traits are to a large extent dependent on an organisms underlying condition. Conclusions drawn from studies of sperm diversification between natural populations are reinforced by experimental evolution studies of sperm morphology in laboratory populations, as these studies address the evolvability of sperm traits and the nature of selection underlying sperm diversification. Furthermore, a discussion of evolutionary causes and consequences of sperm diversification, along with suggestions of fruitful areas for future exploration is presented.

Benefits of Polyandry: A Life History Perspective

Bateman’s principle has been widely interpreted to imply that females gain no fitness benefits from polyandry (Bateman, 1948) and, therefore, should not be expected to mate multiply (here defined as mating with more than one male). Nevertheless, it is increasingly clear that females of many, if not most, taxa do copulate with multiple males (e.g. Birkhead and Wier, 1998). Moreover, polyandry is widespread despite considerable costs, including wasted time and energy, increased risk of predation and disease, potential damage caused by male seminal fluids and copulatory organs, and even death (Keller and Reeve, 1995; Eberhard, 1996). Despite these associated costs, females of diverse taxa not only accept several mates but also actively solicit multiple copulations in many instances (Birkhead and Moller, 1998). As evidence of diverse potential benefits associated with polyandry now accumulates, the assumption that females should not mate multiply because they cannot increase offspring numbers by doing so appears questionable. Importantly, since females have greater potential than males to influence the quality of their offspring, and investment in current reproduction has consequences for future reproductive attempts, they should be expected to optimise offspring numbers rather than maximise numbers produced in any given reproductive attempt (Roff, 1992; Stearns, 1992). Moreover, the relationship between female lifetime reproductive success and offspring numbers and/or size may not be as straightforward as is generally assumed (e.g. Madsen and Shine, 1998; Stockley and Macdonald, 1998). To suggest that females should not mate multiply simply because they cannot increase offspring numbers in a given reproductive attempt by doing so is therefore to confuse the currency of male and female fitness, and thereby to considerably under-estimate the complexity of female reproductive strategies.

The role of genotype-by-environment interactions in sexual selection

Genotype‐by‐environment interactions (GxEs) in naturally selected traits have been extensively studied, but the impact of GxEs on sexual selection has only recently begun to receive attention. Here, we review recent models and consider how GxEs might affect the evolution of sexual traits through influencing sexual signal reliability and also how GxEs may influence variation in sexually selected traits and the process of reproductive isolation. We then assess the current empirical literature on GxEs in sexual selection and conclude by highlighting areas that need additional work. Research on GxEs and sexual selection is an important new area of study for the discipline, which has largely focused on relatively simple mate choice/competition scenarios to date. Investigators now need to apply this knowledge to more complex, but realistic, situations, to more fully explore the evolution of sexual traits, and in this review we suggest potentially useful directions for future research.

Superior sperm competitors sire higher-quality young

The evolution of polyandry remains controversial. This is because, unlike males, in many cases multiple mating by females does not increase fecundity and inevitably involves some costs. As a result, a large number of indirect benefit models have been proposed to explain polyandry. One of these, the good sperm hypothesis, posits that high–quality males are better sperm competitors and sire higher–quality offspring. Hence, by mating multiply, females produce offspring of superior quality. Despite being potentially widely applicable across species, this idea has received little attention. In a laboratory experiment with yellow dung flies ( Scathophaga stercoraria ) we found that males that were more successful in sperm competition also had offspring that developed faster. There was no relationship between paternal success in sperm competition and the ability of offspring to survive post–emergence starvation. Since faster development times are likely to be advantageous in this species, our data provide some support for polyandry evolving as a means of producing higher–quality offspring via sperm competition.

INBREEDING, INBREEDING DEPRESSION AND EXTINCTION

Inbreeding is unavoidable in small, isolated populations and can cause substantial fitness reductions compared to outbred populations. This loss of fitness has been predicted to elevate extinction risk giving it substantial conservation significance. Inbreeding may result in reduced fitness for two reasons: an increased expression of deleterious recessive alleles (partial dominance hypothesis) or the loss of favourable heterozygote combinations (overdominance hypothesis). Because both these sources of inbreeding depression are dependent upon dominance variance, inbreeding depression is predicted to be greater in life history traits than in morphological traits. In this study we used replicate inbred and control lines of Drosophila simulans to address three questions:1) is inbreeding depression greater in life history than morphological traits? 2) which of the two hypotheses is the major underlying cause of inbreeding depression? 3) does inbreeding elevate population extinction risk? We found that inbreeding depression was significantly greater in life history traits compared to morphological traits, but were unable to find unequivocal support for either the overdominance or partial dominance hypotheses as the genetic basis of inbreeding depression. As predicted, inbred lines had a significantly greater extinction risk.

GENETIC ARCHITECTURE OF METABOLIC RATE: ENVIRONMENT SPECIFIC EPISTASIS BETWEEN MITOCHONDRIAL AND NUCLEAR GENES IN AN INSECT

The extent to which mitochondrial DNA (mtDNA) variation is involved in adaptive evolutionary change is currently being reevaluated. In particular, emerging evidence suggests that mtDNA genes coevolve with the nuclear genes with which they interact to form the energy producing enzyme complexes in the mitochondria. This suggests that intergenomic epistasis between mitochondrial and nuclear genes may affect whole‐organism metabolic phenotypes. Here, we use crossed combinations of mitochondrial and nuclear lineages of the seed beetle Callosobruchus maculatus and assay metabolic rate under two different temperature regimes. Metabolic rate was affected by an interaction between the mitochondrial and nuclear lineages and the temperature regime. Sequence data suggests that mitochondrial genetic variation has a role in determining the outcome of this interaction. Our genetic dissection of metabolic rate reveals a high level of complexity, encompassing genetic interactions over two genomes, and genotype × genotype × environment interactions. The evolutionary implications of these results are twofold. First, because metabolic rate is at the root of life histories, our results provide insights into the complexity of life‐history evolution in general, and thermal adaptation in particular. Second, our results suggest a mechanism that could contribute to the maintenance of nonneutral mtDNA polymorphism.

Costs and benefits of evolving under experimentally enforced polyandry or monogamy

Abstract Reproduction has classically been viewed as a predominantly cooperative process. However, over the last 20 years this concept has steadily yielded ground to one of continual conflict in which the interests of the sexes are typically discordant. Within this framework, males and females are seen to be locked into a perpetual arms race, each adaptation by one sex promoting the evolution of countermeasures in the other sex. However, under strict genetic monogamy, the interests of the sexes become congruent, and hence antagonistic coevolution does not occur. We subjected the fly Sepsis cynipsea, a species with conspicuous sexual conflict, to experimentally enforced monogamy or polyandry for 29 generations and evaluated the microevolutionary consequences. We found that there were longevity costs to females consistent with sexually antagonistic coevolution. However, our measure of female fitness, offspring emergence, did not differ between treatments, even though life‐history characters such as fertility and fecundity did. Results are discussed in terms of costs and benefits of sexual selection and sexual conflict.

Monogamy and the Battle of the Sexes

Sexual conflict has been suggested to be important in the evolution of reproductive traits, with much recent theoretical and empirical evidence emphasizing its role in generating sexually antagonistic coevolution in the context of promiscuous mating. Here we shift attention to the role of sexual conflict in a monogamous mating context. Conflicts can arise, for example, when males are successful in imposing monandry at a cost to female fitness, or when females impose monogyny on males. Conflict over remating can also generate monogamy. For example, when males invest heavily in attempting to impose female monandry, the cost of their investment may prevent them from securing additional mates. We emphasize that sexual conflicts need not always generate sexually antagonistic coevolution, and that it is important to consider whether mating decisions are controlled primarily by males or females. Finally, we briefly discuss approaches to distinguish between conflict and classical modes of sexual selection, as this highlights difficulties associated with deciding whether monogamy is enforced by one sex or the other. We suggest that documenting the current fitness consequences of mate choice and mating patterns provides insight into the relative importance of classic and conflict modes of selection.