Sexual selection on condition-dependent traits

Due to immediate fitness benefits, males tend to maximize their investment in ornaments or armaments involved in mate acquisition, and in ejaculate size and quality that can influence competitive fertilization success among rival males. However, these traits tend to be energetically costly, so that males with limited resources available are constrained in their investment, thereby having a fitness disadvantage. Several theoretical models predict that the condition-dependent expression of such costly traits allows females to assess the underlying genetic quality of males and gain genetic benefits for their offspring when mating with the highest-quality males (those with the most exaggerated traits). However, a genetic link between trait expression and male genetic quality has rarely been tested, and nearly nothing is known about the level of condition dependence in postmating sexual traits and how it relates to fitness outcomes. Using quantitative genetic crossing designs in Drosophila melanogaster as a model system, we are addressing the following goals:

• Quantify genetic variation in male and female quality
• Quantify condition dependence of sexual and non-sexual traits
• Examine intensity of sexual selection on traits relative to their condition dependence and quantify the indirect fitness consequences

In parallel, using cross-generational experiments, we are testing new theoretical models of sexual selection and condition dependence that are based on non-genetic transmission of male condition effects to the next generation.

Mechanisms underlying postcopulatory sexual selection and reproductive isolation in Drosophila

We are using Drosophila species as model organisms and apply genetic engineering approaches (i.e., fly populations transformed to produce sperm with green or red fluorescently tagged heads) to study the adaptive significance of intraspecific variation in ejaculate traits. This unique research material enables direct visualization of sperm behavior and fate within their selective environment (i.e., the female reproductive tract) while distinguishing between the sperm from competing males (see VIDEO). So far, our research has demonstrated that (1) males adjust their ejaculates depending on the mating status and reproductive quality of the female; (2) multiple ejaculate traits (e.g., sperm length, velocity and number) are under strong genetic control and, collectively, determine competitive fertilization success, with different ejaculate traits being critical at different stages after female remating; and (3) females can influence the outcome of the competition among ejaculates. More recently, we have also explored the adaptive significance and underlying mechanisms of genetic variation in male × male × female interactions.

In parallel, we have extensively investigated the divergence of the processes underlying conspecific sperm precedence and reproductive isolation among sibling species D. simulans and D. mauritiana. Females of these species show significant differences in the way they store and utilize sperm from different males. Importantly, when males of these different species compete for fertilization in the same female (i.e. conspecific and heterospecific mating), females show a clear preference for sperm of their conspecific mate through differential sperm storage and use. Diversifying (allopatric) postcopulatory sexual selection thus seems to quickly result in reproductive isolation. Combined with the detailed intraspecific examination, our results greatly advance our knowledge of the fundamental microevolutionary processes underlying the important macroevolutionary patterns of biodiversity, which are receiving growing attention in studies of sexual selection.

Thermal fertility

Insects and other ectothermic species, whose physiology and metabolism are governed by ambient temperatures, are particularly vulnerable to the increasingly frequent and intense heat events. As fertility is more sensitive to thermal stress than survival, we are studying the thermal fertilit limits and processes underlying thermal fertility loss in both males and females exposed to sublethal temperature stress, using experimental work on insect model systems. In parallel, we are actively collaborating on various meta-analyses on the topic within the European Thermal Fertility Network, an ESEB-sponsored Special Topics Network, to gain a broader and more general understanding of these patterns.

Within-male sperm selection: The role of genetic variation among 'sibling' sperm

That sperm quality varies widely between individuals is no surprise. But what about different sperm of a given male? Only a small fraction of all sperm transferred will ever reach the ovum. Is this a random selection or are some sperm simply more likely to get there? Since each sperm only carries the haploid genome, it will pass either the maternal or paternal allele on to the next generation. Any genetic differences that could affect sperm quality and thus the likelihood of fertilization could promote selection for these variants. However, to date, clear-cut experimental evidence is limited. We are developing a system in Drosophila fruit flies that will allow us to unambiguously detect haploid selection if it exists. Genes that are expressed post-meiotically (i.e. at the haploid stage) are the most likely targets of haploid selection as these they are less likely to synchronize gene products through exchange via cytoplasmic bridges. Therefore, we use genetic manipulation to fluorescently label different alleles of the same gene. If expressed post-meiotically, fluorescent colours should be mixed, otherwise both colours would be found in each sperm cell. We combine this approach with quantitative PCR techniques of wild-type flies to test how sperm are used by females after mating with a heterozygous male.

Microbial effects on host reproduction

Phenotypes are shaped by their underlying genes, their environment and, as is becoming increasingly clear, by the microbes living in and on them (i.e., microbiota). Particularly the gut microbiota has emerged as an influential contributor to nearly any aspect of its host's life. Sexually transmitted pathogens also play a pivotal role and are extensively studied in both medicine and evolutionary ecology. Surprisingly little is known, however, about the influence of commensal microbes on their host's reproductive health, and, if sexually transmitted, how they interact with the microbiota of their host's sexual partners. Such interactions could have profound fitness consequences for both mates, either directly or mediated by any modulation of the reproductive function. Changes in the reproductive performance could be particularly consequential for males in species in which females mate multiply and thus cause sperm from different males to compete for fertilization. We are studying how the diversity and composition of commensal bacteria influence male reproductive investments and fitness, using wild-caught and lab-reared Drosophila as a study system. We further explore the extent of sexual transmission of bacteria and manipulate the microbial composition to study the effect of representative strains on various male reproductive traits, from sperm quality or composition of the seminal fluid to competitive fertilization success.

Sexual selection and sexual dimorphism in Drosophila prolongata

Drosophila prolongata is quite an exception among drosophilid flies, but remains almost entirely unstudied. Not only are males larger than females, but they also have greatly exaggerated forelegs that they use in both male-male contests and to court females. In addition, they show elaborate courtship behaviour, and males can 'steal' females from their rivals (see VIDEO). With these morphological and behavioural characteristics being likely to have evolved under sexual selection, we want to understand their fitness consequences, the selective process underlying their variation or trade-offs with other reproductive traits. To this end, we will use experimental, morphological, physiological and molecular approaches.

Trade-offs among reproductive investments

Whatever resources an individual invests in one trait, it cannot invest in others. Consequently, trade-offs in resource allocation are often predicted. However, comparisons between individuals or species can become more complicated, because some may simply have more resources available to invest overall than others, which can result in positive rather than negative relationships between traits. Similarly, some traits can be positively related and, jointly, trade off against other, possibly unmeasured traits. We are interested in understanding how different, energetically costly traits are associated with one another and how selection shapes these relationships. We are focusing primarily on combinations of reproductive traits, for example sperm number vs. sperm size or premating vs. postmating sexual traits (e.g., male weapons vs. testes), given that males attempt to maximize their investment in all these traits due to their direct fitness benefits.

In recent work using meta-analytical tools, we have shown that the trade-off between sperm size and number depends on the mechanism of postmating sexual selection and the space at the site of fertilization relative to the numbers of sperm competing. Selection in large organisms tends to disproportionately favour sperm number over sperm length, because sperm risk being lost or diluted in the spacious female reproductive tract. Small organisms, with limited space, tend to show a reversed pattern. Transferring more competitive sperm, able to displace rival sperm from storage, appears to be a better strategy than simply increasing sperm quantity and having excess sperm never even reaching storage. Similarly, we have shown how the male's ability to monopolize females changes relative allocation to pre- and postmating sexual traits. Relative to premating weapons, testes become increasingly important as the ability of warding off rival males declines and the risk of sperm competition increases. So, the relationship between pre- and postmating sexual traits can vary between strongly positive and strongly negative.

Evolution of reproductive traits in birds

Our earlier research also focused on understanding the processes underlying the stunning diversification in sperm morphology and its associations with sperm function in passerine birds. For example, in comparative studies, focusing primarily of New World Blackbirds (Icteridae), we have shown how sperm morphology is shaped through postcopulatory sexual selection, possibly because longer sperm can swim faster (and thus potentially have a fertilization advantage). Associated with this variation in sperm morphology and selection for longer and greater numbers of sperm through sperm competition, we also found adaptations in testicular morphology and spermatogenic efficiency. Importantly, various constraints in sperm production can result in trade-offs between sperm size and number, but the way these trade-offs manifest themselves depends on the conditions at the site of fertilization and the processes of sperm competition.

We have also documented systematic variation in sperm morphology across the species range of the red-winged blackbird (Agelaius phoeniceus). This species exhibits among-population diversity in mating systems, and our results suggest that the sperm diversity may track the expansion of this species from its origin. Finally, although sperm size and shape are typically assumed to be consistent within males, we have shown in the same species that sperm morphology, velocity and quantity can be phenotypically and adaptively plastic across the breeding season.