Sexual selection shapes development and maturation rates inDrosophila

Abstract

Explanations for the evolution of delayed maturity usually invoke trade-offs mediated by growth, but processes of reproductive maturation continue long after growth has ceased. Here, we tested whether sexual selection shapes the rate of posteclosion maturation in the fruit fly Drosophila melanogaster. We found that populations maintained for more than 100 generations under a short generation time and polygamous mating system evolved faster posteclosion maturation and faster egg-to-adult development of males, when compared to populations kept under short generations and randomized monogamy that eliminated sexual selection. An independent assay demonstrated that more mature males have higher fitness under polygamy, but this advantage disappears under monogamy. In contrast, for females greater maturity was equally advantageous under polygamy and monogamy. Furthermore, monogamous populations evolved faster development and maturation of females relative to polygamous populations, with no detectable trade-offs with adult size or egg-to-adult survival. These results suggest that a major aspect of male maturation involves developing traits that increase success in sexual competition, whereas female maturation is not limited by investment in traits involved in mate choice or defense against male antagonism. Moreover, rates of juvenile development and adult maturation can readily evolve in opposite directions in the two sexes, possibly implicating polymorphisms with sexually antagonistic pleiotropy.

Sexual conflict drives male manipulation of female postmating responses inDrosophila melanogaster

“…Differences in investment in SFP gene expression between males from the two evolutionary regimes were therefore visible at the time point marking the beginning of the male–female interaction period over the course of experimental evolution but absent at the end of the interaction period. The relative immaturity in the pattern of expression of SFP genes in M males is consistent with what has been previously found when examining gene expression in the heads of M males (80) and suggests the possibility of a generalized maturation deficit under selection in the monogamous regime.…”

“…Previous studies examining mature adults found that D. pseudoobscura males evolved under monogamy invested less in the accessory glands (77), while D. melanogaster males evolving at different intensities of sexual competition did not differ in accessory gland investment (78). Because of the importance of early adult maturation in the sexual success of D. melanogaster males, both in general (79) and within the evolutionary regimes (80), we took a different approach and assessed the growth of the accessory gland by measuring its size across the first 4 d post eclosion. Male accessory glands more than doubled in size in the first few days (age: χ 2 1 = 686.8, P < 0.0001), with growth slowing as males matured (age 2 : χ 2 1 = 162.2, P < 0.0001).…”

“…Furthermore, past work directly estimating N e based on molecular markers in experimental populations with differing intensities of sexual competition found no difference between monogamous and promiscuous populations (82). Diminished M male effects on females could also have arisen if deleterious variation was purged less efficiently from these populations (83, 84), but past work with these populations found no evidence for this (42, 80). Our findings therefore support the hypothesis that a substantial part of male effects on the female postmating response are detrimental to females and/or carry a cost to male nonsexual fitness.…”

Population-, sex- and individual level divergence in life-history and activity patterns in an annual killifish

“…These sex-associated differences illustrate the importance of including both sexes when studying life-history responses. Whereas the negative association between female maturation rate and adult body size is broadly supported in literature, this is far less so for males (Hollis, Keller & Kawecki, 2016). Likely, there are additional fitness advantages associated with early male maturation, such as accommodating aggressive male competition for mates (Reichard, Polačik & Sedláček, 2009) that drive selection for early maturation.…”

“…Especially in short-lived ponds, demographic modelling illustrates that early maturation can be an important determinant of long term population growth rates for organisms with a life cycle similar to that of N. furzeri (Pinceel et al, 2016). In addition, life-history theory predicts a higher maturation rate to be offset by a reduced adult body size (Hollis, Keller & Kawecki, 2016). Although there was a trend for faster maturation of females from short-lived ponds and females from short-lived ponds were smaller as adults than females from long-lived ponds, an opposite association was found for male maturation time and males from different population types did not differ in adult body size.…”