Quantitative genetic insights into the coevolutionary dynamics of male and female genitalia

The spectacular variability that typically characterizes male genital traits has largely been attributed to the role of sexual selection. Among the evolutionary mechanisms proposed to account for this diversity, two processes in particular have generated considerable interest. On the one hand, females may exploit postcopulatory mechanisms of selection to favour males with preferred genital traits (cryptic female choice; CFC), while on the other hand females may evolve structures or behaviours that mitigate the direct costs imposed by male genitalia (sexual conflict; SC). A critical but rarely explored assumption underlying both processes is that male and female reproductive traits coevolve, either via the classic Fisherian model of preference-trait coevolution (CFC) or through sexually antagonistic selection (SC). Here, we provide evidence for this prediction in the guppy (Poecilia reticulata), a polyandrous livebearing fish in which males transfer sperm internally to females via consensual and forced matings. Our results from a paternal half-sibling breeding design reveal substantial levels of additive genetic variation underlying male genital size and morphology—two traits known to predict mating success during non-consensual matings. Our subsequent finding that physically interacting female genital traits exhibit corresponding levels of genetic (co)variation reveals the potential intersexual coevolutionary dynamics of male and female genitalia, thereby fulfilling a fundamental assumption underlying CFC and SC theory.     

Mutation rates and the evolution of germline structure

Genome sequencing studies of de novo mutations in humans have revealed surprising incongruities in our understanding of human germline mutation. In particular, the mutation rate observed in modern humans is substantially lower than that estimated from calibration against the fossil record, and the paternal age effect in mutations transmitted to offspring is much weaker than expected from our long-standing model of spermatogenesis. I consider possible explanations for these discrepancies, including evolutionary changes in life-history parameters such as generation time and the age of puberty, a possible contribution from undetected post-zygotic mutations early in embryo development, and changes in cellular mutation processes at different stages of the germline. I suggest a revised model of stem-cell state transitions during spermatogenesis, in which ‘dark’ gonial stem cells play a more active role than hitherto envisaged, with a long cycle time undetected in experimental observations. More generally, I argue that the mutation rate and its evolution depend intimately on the structure of the germline in humans and other primates.This article is part of the themed issue ‘Dating species divergences using rocks and clocks''.     

Gamete evolution and sperm numbers: sperm competition versus sperm limitation

Both gamete competition and gamete limitation can generate anisogamy from ancestral isogamy, and both sperm competition (SC) and sperm limitation (SL) can increase sperm numbers. Here, we compare the marginal benefits due to these two components at any given population level of sperm production using the risk and intensity models in sperm economics. We show quite generally for the intensity model (where N males compete for each set of eggs) that however severe the degree of SL, if there is at least one competitor for fertilization (N − 1 ≥ 1), the marginal gains through SC exceed those for SL, provided that the relationship between the probability of fertilization (F) and increasing sperm numbers (x) is a concave function. In the risk model, as fertility F increases from 0 to 1.0, the threshold SC risk (the probability q that two males compete for fertilization) for SC to be the dominant force drops from 1.0 to 0. The gamete competition and gamete limitation theories for the evolution of anisogamy rely on very similar considerations: our results imply that gamete limitation could dominate only if ancestral reproduction took place in highly isolated, small spawning groups.     

Patterns of sperm damage in Chernobyl passerine birds suggest a trade-off between sperm length and integrity

Interspecific variation in sperm size is enigmatic, but generally assumed to reflect species-specific trade-offs in selection pressures. Among passerine birds, sperm length varies sevenfold, and sperm competition risk seems to drive the evolution of longer sperm. However, little is known about factors favouring short sperm or constraining the evolution of longer sperm. Here, we report a comparative analysis of sperm head abnormalities among 11 species of passerine bird in Chernobyl, presumably resulting from chronic irradiation following the 1986 accident. Frequencies of sperm abnormalities varied between 15.7 and 77.3% among species, more than fourfold higher than in uncontaminated areas. Nonetheless, species ranked similarly in sperm abnormalities in unpolluted areas as in Chernobyl, pointing to intrinsic factors underlying variation in sperm damage among species. Scanning electron microscopy of abnormal spermatozoa revealed patterns of acrosome damage consistent with premature acrosome reaction. Sperm length, but not sperm competition risk explained variation in sperm damage among species. This suggests that longer spermatozoa are more susceptible to premature acrosome reaction. Therefore, we hypothesize a trade-off between sperm length and sperm integrity affecting sperm evolution in passerine birds.     

Evolution of intra‐ejaculate sperm interactions: do sperm cooperate?

Sperm are often considered to be individuals, in part because of their unique genetic identities produced as a result of synapsis during meiosis, and in part due to their unique ecology, being ejected away from the soma to continue their existence in a foreign environment. Selection at the level of individual sperm has been suggested to explain the evolution of two enigmatic sperm phenotypes: sperm heteromorphism, where more than one type of sperm is produced by a male, and sperm conjugation, where multiple sperm join together for motility and transport through the female reproductive tract before dissociation prior to fertilization. In sperm heteromorphic species, only one of the sperm morphs typically participates in fertilization, with the non‐fertilizing “parasperm” being interpreted as reproductive altruists. Likewise, in species with sperm conjugation, high levels of sperm mortality have been suggested to be required for conjugate break‐up and this has been considered evidence of kin‐selected altruism. However, it is unclear if sperm possess the heritable variation in fitness (i.e. are individuals) required for the evolution of cooperation. We investigate the question of sperm individuality by focusing on how sperm morphology is determined and how sperm conjugates are formed. Concentrating on sperm conjugation, we discuss functional hypotheses for the evolutionary maintenance of this remarkable trait. Additionally, we speculate on the potential origins of sperm heteromorphism and conjugation, and explore the diversification and losses of these traits once they have arisen in a lineage. We find current evidence insufficient to support the concept of sperm control over their form or function. Thus, without additional evidence of haploid selection (i.e. sperm phenotypes that reflect their haploid genome and result in heritable differences in fitness), sperm heteromorphism and conjugation should be interpreted not as cooperation but rather as traits selected at the level of the male, much like other ejaculatory traits such as accessory gland proteins and ejaculate size.     

Vicariance, climate change, anatomy and phylogeny of Restionaceae

Cutler suggested almost 30 years ago that there was convergent evolution between African and Australian Restionaceae in the distinctive culm anatomical features of Restionaceae. This was based on his interpretation of the homologies of the anatomical features, and these are here tested against a 'supertrec' phylogeny, based on three separate phvlogenies. The first is based on morphology and includes all genera; the other two are based on molecular sequences from the chloroplast genome-, one covers the African genera, and the other tin-Australian genera. This analysis corroborates Cutler's interpretation of convergent evolution between African and Australian Restionaceae. However, it indicates that for the Australian genera, the evolutionary pathway of the culm anatomy is much more complex than originally thought. In the most likely scenario, the ancestral Restionaceae have protective cells derived from the chlorenchyma. These persist in African Restionaceae, but are soon lost in Australian Restionaceae. Pillar cells and sclerenchyma ribs evolve early in the diversification of Australian Restionaceae, but are secondarily lost numerous times. In some of the reduction cases, the result is a very simple culm anatomy, which Cutler had interpreted as a primitively simple culm type, while in other cases it appears as if the functions of the ribs and pillars may have been taken over by a new structure, protective cells developed from epidermal, rather than chlorenchyma, cells. Cutler suggested that this convergent evolution might have been in response to Tertiary climatic deterioration, but this study finds no strong corroborating evidence for this.