Co-evolution of male and female reproductive traits across the Bruchidae (Coleoptera)

1. Despite the obvious importance of spermatozoa to individual reproductive success a general explanation of variation in spermatozoan form and function is still lacking. In species with internal fertilization, sperm not only have to interact with the physical and biochemical environment of the female reproductive tract, but frequently face competition from the sperm of rival males. Both sperm competition theory and adaptation to the selective environment of the female reproductive tract have been implicated in the evolution of spermatozoan morphological diversity. 2. Using the comparative method, we examine variation in sperm length in relation to (i) sperm competition intensity (as measured by relative testis size) and (ii) female reproductive characters, across 15 species of beetle belonging to the family Bruchidae. 3. Stepwise multiple regression within a phylogenetic framework revealed sperm length to be positively correlated with female spermathecal duct length and negatively related to spermathecal volume, but not testes size, indicating that the female reproductive environment rather than sperm competition per se exerts selection on sperm length in this taxonomic group. 4. A positive association between testes volume and the volume of the female spermatheca was also evident suggesting correlated evolution of these traits. 5. A number of models of sexual selection could lead to the correlated evolution of male and female reproductive characters, although the underlying mechanisms of cause and effect remain elusive. Divergence between species (and populations) in primary reproductive traits is likely to present a significant barrier to hetero-specific fertilization, and thus contribute to reproductive isolation

Mechanisms underlying the sperm quality advantage in sperm competition and cryptic female choice in Drosophila melanogaster

Contrary to early predictions of sperm competition theory, postcopulatory sexual selection favoring increased investment per sperm (e.g., sperm size, sperm quality) has been demonstrated in numerous organisms. Recent findings reveal that sperm production strategies are highly variable, with males of some species producing relatively few, giant sperm. We empirically demonstrate for Drosophila melanogaster that both sperm quality and sperm quantity independently contribute to competitive male fertilization success. The interaction between sperm quality and quantity suggests an internal positive reinforcement on selection for sperm quality, with selection predicted to intensify as investment per sperm increases and the number of sperm competing declines. The mechanism underlying the sperm quality advantage is elucidated through examination of the relationship between female sperm-storage organ morphology and the differential organization of different length sperm within the organ. Our results exemplify that primary sex cells can bear secondary sexual straits

The evolution of harm: effect of sexual conflicts and population size

Conflicts of interest between mates can lead to the evolution of male traits reducing female fitness and to coevolution between the sexes. The rate of adaptation and counter-adaptation is constrained by the intensity of selection and its efficiency, which depends on drift and genetic variability. This leads to the largely untested prediction that coevolutionary adaptations such as those driven by sexual conflict should evolve faster in large populations where the response to selection is stronger and sexual selection is more intense. We test this using the bruchid beetle Callosobruchus maculatus, a species with well documented male harm. Whilst most experimental evolution studies remove sexual conflicts, we reintroduce sexual conflict in populations where it has been experimentally removed. Both population size and standing genetic variability were manipulated in a factorial experimental design. After 90 generations of relaxed conflict (monogamy), the reintroduction of sexual conflicts for 30 generations favoured males that harmed females and females more resistant to the genital damage inflicted by males. Large population size rather than high initial genetic variation allowed males to evolve faster and become more harmful. Sexual selection thus creates conditions where males benefit from harming females and this selection is more effective in larger populations

The life history of Drosophila sperm involves molecular continuity between male and female reproductive tracts

This research was funded by the National Science Foundation (DEB 1655840 to S.D., S.P., and M.F.W.), the National Institutes of Health (NICHD R21HD088910 to S.D., S.P. and M.F.W. and R37/R01HD038921 to M.F.W.), and a generous gift from Mike and Jane Weeden to Syracuse University.Interactions between sperm and the female reproductive tract (FRT) are critical to reproductive success and yet are poorly understood. Because sperm complete their functional maturation within the FRT, the life history of sperm is likely to include a molecular “hand-off” from males to females. Although such intersexual molecular continuity is likely to be widespread among all internally fertilizing species, the identity and extent of female contributions are largely unknown. We combined semiquantitative proteomics with sex-specific isotopic labeling to catalog the posttesticular life history of the sperm proteome and determine the extent of molecular continuity between male and FRTs. We show that the Drosophila melanogaster sperm proteome undergoes substantial compositional changes after being transferred to the FRT. Multiple seminal fluid proteins initially associate with sperm, but most become undetectable after sperm are stored. Female-derived proteins also begin to associate with sperm immediately after mating, and they comprise nearly 20% of the postmating sperm proteome following 4 d of storage in the FRT. Female-derived proteins that associate with sperm are enriched for processes associated with energy metabolism, suggesting that female contributions support sperm viability during the prolonged period between copulation and fertilization. Our research provides a comprehensive characterization of sperm proteome dynamics and expands our understanding of the critical process of sperm–FRT interactions.Peer reviewe

Sperm morphology and the evolution of intracellular sperm-egg interactions

This is the final version of the article. Available from Wiley via the DOI in this record.Sperm morphology is incredibly diverse, even among closely related species, yet the coevolution between males and females of fertilization recognition systems is necessary for successful karyogamy (male and female pronuclear fusion). In most species, the entire sperm enters the egg during fertilization so sperm morphological diversity may impact the intracellular sperm–egg interactions necessary for karyogamy. We quantified morphological variation of sperm inside eggs prior to and following karyogamy in several species of Drosophila to understand whether evolution of sperm morphology could influence intracellular sperm–egg interactions (ISEIs). We measured seven parameters that describe ISEIs among species to determine whether these parameters varied both within a species across development and across species at the same developmental stage. We used heterospecific crosses to test the relative role of male origin, female origin, and interaction between the male and female in determining ISEIs. We found that sperm shape changed within a species as development proceeded and, at particular development stages, species varied in some ISEIs. Parental origin had an effect on some ISEIs, with a general trend for a stronger female effect. Overall, our findings identify conserved and variable ISEIs among species and demonstrate the potential to contribute understanding to gamete evolution and development.Leverhulme Trus

Experimental evolution reveals that sperm competition intensity selects for longer, more costly sperm

It is the differences between sperm and eggs that fundamentally underpin the differences between the sexes within reproduction. For males, it is theorized that widespread sperm competition leads to selection for investment in sperm numbers, achieved by minimizing sperm size within limited resources for spermatogenesis in the testis. Here, we empirically examine how sperm competition shapes sperm size, after more than 77 generations of experimental selection of replicate lines under either high or low sperm competition intensities in the promiscuous flour beetle Tribolium castaneum. After this experimental evolution, populations had diverged significantly in their sperm competitiveness, with sperm in ejaculates from males evolving under high sperm competition intensities gaining 20% greater paternity than sperm in ejaculates from males that had evolved under low sperm competition intensity. Males did not change their relative investment into sperm production following this experimental evolution, showing no difference in testis sizes between high and low intensity regimes. However, the more competitive males from high sperm competition intensity regimes had evolved significantly longer sperm and, across six independently selected lines, there was a significant association between the degree of divergence in sperm length and average sperm competitiveness. To determine whether such sperm elongation is costly, we used dietary restriction experiments, and revealed that protein-restricted males produced significantly shorter sperm. Our findings therefore demonstrate that sperm competition intensity can exert positive directional selection on sperm size, despite this being a costly reproductive trait

Nonantagonistic interactions between the sexes revealed by the ecological consequences of reproductive traits

Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/73504/1/j.1420-9101.2004.00779.x.pd

Sperm death and dumping in Drosophila

Mating with more than one male is the norm for females of many species. In addition to generating competition between the ejaculates of different males, multiple mating may allow females to bias sperm use. In Drosophila melanogaster, the last male to inseminate a female sires approximately 80% of subsequent progeny. Both sperm displacement, where resident sperm are removed from storage by the incoming ejaculate of the copulating male, and sperm incapacitation, where incoming seminal fluids supposedly interfere with resident sperm, have been implicated in this pattern of sperm use. But the idea of incapacitation is problematic because there are no known mechanisms by which an individual could damage rival sperm and not their own. Females also influence the process of sperm use, but exactly how is unclear. Here we show that seminal fluids do not kill rival sperm and that any 'incapacitation' is probably due to sperm ageing during sperm storage. We also show that females release stored sperm from the reproductive tract (sperm dumping) after copulation with a second male and that this requires neither incoming sperm nor seminal fluids. Instead, males may cause stored sperm to be dumped or females may differentially eject sperm from the previous mating

Developmental temperature affects the expression of ejaculatory traits and the outcome of sperm competition in Callosobruchus maculatus

The outcome of post-copulatory sexual selection is determined by a complex set of interactions between the primary reproductive traits of two or more males and their interactions with the reproductive traits of the female. Recently, a number of studies have shown the primary reproductive traits of both males and females express phenotypic plasticity in response to the thermal environment experienced during ontogeny. However, how plasticity in these traits affects the dynamics of sperm competition remains largely unknown. Here, we demonstrate plasticity in testes size, sperm size and sperm number in response to developmental temperature in the bruchid beetle Callosobruchus maculatus. Males reared at the highest temperature eclosed at the smallest body size and had the smallest absolute and relative testes size. Males reared at both the high- and low-temperature extremes produced both fewer and smaller sperm than males reared at intermediate temperatures. In the absence of sperm competition, developmental temperature had no effect on male fertility. However, under conditions of sperm competition, males reared at either temperature extreme were less competitive in terms of sperm offence (P2), whereas those reared at the lowest temperature were less competitive in terms of sperm defence (P1). This suggests the developmental pathways that regulate the phenotypic expression of these ejaculatory traits are subject to both natural and sexual selection: natural selection in the pre-ejaculatory environment and sexual selection in the post-ejaculatory environment. In nature, thermal heterogeneity during development is commonplace. Therefore, we suggest the interplay between ecology and development represents an important, yet hitherto underestimated component of male fitness via post-copulatory sexual selection