A genome-wide test for paternal indirect genetic effects on lifespan in Drosophila melanogaster.

Exposing sires to various environmental manipulations has demonstrated that paternal effects can be non-trivial also in species where male investment in offspring is almost exclusively limited to sperm. Whether paternal effects also have a genetic component (i.e. paternal indirect genetic effects (PIGEs)) in such species is however largely unknown, primarily because of methodological difficulties separating indirect from direct effects of genes. PIGEs may nevertheless be important since they have the capacity to contribute to evolutionary change. Here we use Drosophila genetics to construct a breeding design that allows testing nearly complete haploid genomes (more than 99%) for PIGEs. Using this technique, we estimate the variance in male lifespan due to PIGEs among four populations and compare this to the total paternal genetic variance (the sum of paternal indirect and direct genetic effects). Our results indicate that a substantial part of the total paternal genetic variance results from PIGEs. A screen of 38 haploid genomes, randomly sampled from a single population, suggests that PIGEs also influence variation in lifespan within populations. Collectively, our results demonstrate that PIGEs may constitute an underappreciated source of phenotypic variation.

The shared genome is a pervasive constraint on the evolution of sex-biased gene expression.

Males and females share most of their genomes, and differences between the sexes can therefore not evolve through sequence divergence in protein coding genes. Sexual dimorphism is instead restricted to occur through sex-specific expression and splicing of gene products. Evolution of sexual dimorphism through these mechanisms should, however, also be constrained when the sexes share the genetic architecture for regulation of gene expression. Despite these obstacles, sexual dimorphism is prevalent in the animal kingdom and commonly evolves rapidly. Here, we ask whether the genetic architecture of gene expression is plastic and easily molded by sex-specific selection, or if sexual dimorphism evolves rapidly despite pervasive genetic constraint. To address this question, we explore the relationship between the intersexual genetic correlation for gene expression (rMF), which captures how independently genes are regulated in the sexes, and the evolution of sex-biased gene expression. Using transcriptome data from Drosophila melanogaster, we find that most genes have a high rMF and that genes currently exposed to sexually antagonistic selection have a higher average rMF than other genes. We further show that genes with a high rMF have less pronounced sex-biased gene expression than genes with a low rMF within D. melanogaster and that the strength of the rMF in D. melanogaster predicts the degree to which the sex bias of a gene's expression has changed between D. melanogaster and six other species in the Drosophila genus. In sum, our results show that a shared genome constrains both short- and long-term evolution of sexual dimorphism.

Sex differences in aggression: Differential roles of 5-HT2, neuropeptide F and tachykinin.

Despite the conserved function of aggression across taxa in obtaining critical resources such as food and mates, serotonin's (5-HT) modulatory role on aggressive behavior appears to be largely inhibitory for vertebrates but stimulatory for invertebrates. However, critical gaps exist in our knowledge of invertebrates that need to be addressed before definitively stating opposing roles for 5-HT and aggression. Specifically, the role of 5-HT receptor subtypes are largely unknown, as is the potential interactive role of 5-HT with other neurochemical systems known to play a critical role in aggression. Similarly, the influence of these systems in driving sex differences in aggressive behavior of invertebrates is not well understood. Here, we investigated these questions by employing complementary approaches in a novel invertebrate model of aggression, the stalk-eyed fly. A combination of altered social conditions, pharmacological manipulation and 5-HT2 receptor knockdown by siRNA revealed an inhibitory role of this receptor subtype on aggression. Additionally, we provide evidence for 5-HT2's involvement in regulating neuropeptide F activity, a suspected inhibitor of aggression. However, this function appears to be stage-specific, altering only the initiation stage of aggressive conflicts. Alternatively, pharmacologically increasing systemic concentrations of 5-HT significantly elevated the expression of the neuropeptide tachykinin, which did not affect contest initiation but instead promoted escalation via production of high intensity aggressive behaviors. Notably, these effects were limited solely to males, with female aggression and neuropeptide expression remaining unaltered by any manipulation that affected 5-HT. Together, these results demonstrate a more nuanced role for 5-HT in modulating aggression in invertebrates, revealing an important interactive role with neuropeptides that is more reminiscent of vertebrates. The sex-differences described here also provide valuable insight into the evolutionary contexts of this complex behavior.

Effects of developmental environment on signal-preference coupling in a Hawaiian cricket.

Previous work has suggested that developmental temperature influences expression of the adult male calling song of the cricket, a sexually selected mate recognition signal. The role of developmental temperature in shaping female preference functions, and thus its influence on signal-preference coupling has not been investigated. In this study, the effects of developmental temperature are examined in both males and females of the Hawaiian cricket, Laupala cerasina, to determine the degree of signal-preference matching between male song and female preference due to developmental environment. We found that rearing females in different temperature environments affected adult female acoustic preference functions in the same direction as male calling song, thereby influencing variation in adult reproductive behavior in such a way that male and female components remain coordinated. However, we further demonstrate that for male song, the effect of the rearing environment is not permanent but appears only to exert influence for a period of days. This mid-term temperature effect is distinct from the effect of short-term ambient temperature, which influences song in a matter of minutes and has been well documented. Signal-preference coordination, and sexual selection pressures due to mismatching within natural populations, likely will be influenced by nymphal developmental environments of males and females, as well as by adult singing and preference environments.

Coevolution of male mating signal and female preference during early lineage divergence of the Hawaiian cricket, Laupala cerasina.

Sexual selection is a powerful evolutionary force shaping mate choice phenotypes, initiating phenotypic shifts resulting in (or reinforcing) population divergence and speciation when such shifts reduce mating probabilities among divergent populations. In the Hawaiian cricket genus Laupala, pulse rate of male calling song, a conspicuous mating signal, differs among species, potentially behaving as a speciation phenotype. Populations of the widespread species Laupala cerasina show variation in pulse rate. We document the degree of population differentiation in three features of calling song: pulse rate, pulse duration, and carrier frequency. All show significant population differentiation, with pulse rate showing the greatest heterogeneity. A Mantel test found no relationship between geographic distance and pulse rate divergence, indicating that a simple model of greater divergence with increasing distance cannot explain the observed pattern of differentiation. We demonstrate that female preference functions for pulse rate are unimodal, and that preference means show significant differentiation among populations. Furthermore, estimates of pulse rate preference correlate significantly with mean pulse rates across populations, indicating song and preference coevolve in a stepwise manner. This correlated divergence between signal and preference suggests that sexual selection facilitates the establishment of sexual isolation, reduced gene flow, and population differentiation, prerequisites for speciation.