Postmating transcriptional changes in reproductive tracts of con- and heterospecifically mated Drosophila mojavensis females

Abstract

In internally fertilizing organisms, mating involves a series of highly coordinated molecular interactions between the sexes that occur within the female reproductive tract. In species where females mate multiply, traits involved in postcopulatory interactions are expected to evolve rapidly, potentially leading to postmatingprezygotic (PMPZ) reproductive isolation between diverging populations. Here, we investigate the postmating transcriptional response of the lower reproductive tract of Drosophila mojavensis females following copulation with either conspecific or heterospecific (Drosophila arizonae) males at three time points postmating. Relatively few genes (15 total) were differentially regulated in the female lower reproductive tract in response to conspecific mating. Heterospecifically mated females exhibited significant perturbations in the expression of the majority of these genes, and also down-regulated transcription of a number of others, including several involved in mitochondrial function. These striking regulatory differences indicate failed postcopulatory molecular interactions between the sexes consistent with the strong PMPZ isolation observed for this cross. We also report the transfer of male accessory-gland protein (Acp) transcripts from males to females during copulation, a finding with potentially broad implications for understanding postcopulatory molecular interactions between the sexes.n internally fertilizing organisms, the female reproductive tract serves as the arena for a series of highly coevolved molecular interactions between the sexes that are critical for successful reproduction (1, 2). Postcopulatory interactions should further increase in complexity in species in which females mate with more than one male, as intense sexual selection propels the rapid evolution of traits mediating female choice, male competitive ability, and sexual conflict (3,4). This, in turn, may facilitate divergence of such traits between populations following different coevolutionary trajectories, leading to postmating-prezygotic (PMPZ) reproductive isolation (5). Consistent with these expectations are the rapid evolution of morphological and molecular reproductive traits associated with postcopulatory processes (6) and the recognition that PMPZ barriers can serve as potent and rapidly evolving forms of reproductive isolation (5).The availability of genomic resources for an increasing number of species provides a platform for elucidating the molecular basis of postcopulatory molecular interactions between males and females. For example, recent genomic studies on Drosophila melanogaster (7-14), Anopheles gambiae (15), and Apis mellifera (16, 17) have begun to characterize the female postmating response by identifying changes in the transcriptome and/or proteome of mated females. In D. melanogaster, sperm or other specific components of the seminal fluid are known to induce some of these changes, which ultimately trigger physiological responses in females (18). Male accessory-gland proteins (Acps), in part...

Dynamic digestive physiology of a female reproductive organ in a polyandrous butterfly

“…Research on this front is critical for understanding how these traits mediate male-female interactions as well as how they function across individual female life histories. However, with the exception of a few recent studies in Drosophila melanogaster (Bono et al, 2011;Kelleher and Pennington, 2009;Mack et al, 2006;McGraw et al, 2008), such information is largely lacking for even well-studied organisms.…”

Polyandry and sex-specific gene expression

“…They are therefore subject to particularly strong male-specific selection, which may explain why ACPs are among the most rapidly evolving proteins in the genome [103,104]. Females show a profound transcriptomic response to ACPs [41,46,47], and female-specific selection could act to make females resistant to male manipulation that is harmful to female fitness. Because of this, we might predict that ACPs would evolve more rapidly under polyandry than both monandry and monogamy.…”

“…Beyond the brain, mating elicits a huge response in gene expression in the female reproductive tract [37,41,42]. Part of this is due to the female's innate transcriptomic preparations for embryo provisioning [43].…”

“…Finally, part of the changes in the female reproductive tract is in response to manipulative proteins from the male transcriptome in the form of accessory gland proteins (ACPs) [41,46,47], which stimulate female oogenesis and ovulation, as well as impede female remating [47]. ACPs appear to be involved in inter-locus sexual conflict, which involves interactions between antagonistic alleles at two or more loci in males and females, and so they are also discussed in §6.…”

Reproductive isolation in the Elegans-Group of Caenorhabditis

“…In species with internal fertilization, responses of the reproductive tract to interspecific sperm also may limit or prevent fertilization after mating has occurred. In some combinations of Drosophila species, the insemination reaction may serve this purpose [48][49][50].…”