Rapid divergence of the male reproductive proteins in the Drosophila dunni group and implications for postmating incompatibilities between species.
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ABSTRACT:
SUBMITTER: Hill T
PROVIDER: S-EPMC8759818 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Understanding the genetic basis of speciation is a central problem in evolutionary biology. Studies of reproductive isolation have provided several insights into the genetic causes of speciation, especially in taxa that lend themselves to detailed genetic scrutiny. Reproductive barriers have usually been divided into those that occur before zygote formation (prezygotic) and after (postzygotic), with the latter receiving a great deal of attention over several decades. Reproductive barriers that occur after mating but before zygote formation [postmating prezygotic (PMPZ)] are especially understudied at the genetic level. Here, I present a phenotypic and genetic analysis of a PMPZ reproductive barrier between two species of the Drosophila virilis group: D. americana and D. virilis This species pair shows strong PMPZ isolation, especially when D. americana males mate with D. virilis females: ∼99% of eggs laid after these heterospecific copulations are not fertilized. Previous work has shown that the paternal loci contributing to this incompatibility reside on two chromosomes, one of which (chromosome 5) likely carries multiple factors. The other (chromosome 2) is fixed for a paracentric inversion that encompasses nearly half the chromosome. Here, I present two results. First, I show that PMPZ in this species cross is largely due to defective sperm storage in heterospecific copulations. Second, using advanced intercross and backcross mapping approaches, I identify genomic regions that carry genes capable of rescuing heterospecific fertilization. I conclude that paternal incompatibility between D. americana males and D. virilis females is underlain by four or more genes on chromosomes 2 and 5.
| S-EPMC5144975 | biostudies-literature
Project description:Fertility depends, in part, on interactions between male and female reproductive proteins inside the female reproductive tract (FRT) that mediate postmating changes in female behaviour, morphology, and physiology. Coevolution between interacting proteins within species may drive reproductive incompatibilities between species, yet the mechanisms underlying postmating-prezygotic (PMPZ) isolating barriers remain poorly resolved. Here, we used quantitative proteomics in sibling Drosophila species to investigate the molecular composition of the FRT environment and its role in mediating species-specific postmating responses. We found that (i) FRT proteomes in D. simulans and D. mauritiana virgin females express unique combinations of secreted proteins and are enriched for distinct functional categories, (ii) mating induces substantial changes to the FRT proteome in D. mauritiana but not in D. simulans, and (iii) the D. simulans FRT proteome exhibits limited postmating changes irrespective of whether females mate with conspecific or heterospecific males, suggesting an active female role in mediating reproductive interactions. Comparisons with similar data in the closely related outgroup species D. melanogaster suggest that divergence is concentrated on the D. simulans lineage. Our study suggests that divergence in the FRT extracellular environment and postmating response contribute to previously described patterns of PMPZ isolation and the maintenance of species boundaries.
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Project description:Speciation can occur through the presence of reproductive isolation barriers that impede mating, restrict cross-fertilization, or render inviable/sterile hybrid progeny. The D. willistoni subgroup is ideally suited for studies of speciation, with examples of both allopatry and sympatry, a range of isolation barriers, and the availability of one species complete genome sequence to facilitate genetic studies of divergence. D. w. willistoni has the largest geographic distribution among members of the Drosophila willistoni subgroup, spanning from Argentina to the southern United States, including the Caribbean islands. A subspecies of D. w. willistoni, D. w. quechua, is geographically separated by the Andes mountain range and has evolved unidirectional sterility, in that only male offspring of D. w. quechua females × D. w. willistoni males are sterile. Whether D. w. willistoni flies residing east of the Andes belong to one or more D. willistoni subspecies remains unresolved. Here we perform fecundity assays and show that F1 hybrid males produced from crosses between different strains found in Central America, North America, and northern Caribbean islands are reproductively isolated from South American and southern Caribbean island strains as a result of unidirectional hybrid male sterility. Our results show the existence of a reproductive isolation barrier between the northern and southern strains and suggest a subdivision of the previously identified D. willistoni willistoni species into 2 new subspecies.
| S-EPMC5036932 | biostudies-literature
Project description:Fertility depends, in part, on interactions between male and female reproductive proteins inside the female reproductive tract (FRT) that mediate postmating changes in female behavior, morphology, and physiology. Coevolution between interacting proteins within species may drive reproductive incompatibilities between species, yet the mechanisms underlying postmating-prezygotic isolating barriers remain poorly resolved. Here, we used quantitative proteomics in sibling Drosophila species to investigate the molecular composition of the FRT environment and its role in mediating species-specific postmating responses. We found that (1) FRT proteomes in D. simulans and D. mauritiana virgin females express unique combinations of secreted proteins and are enriched for distinct functional categories, (2) mating induces substantial changes to the FRT proteome in D. mauritiana but not in D. simulans, and (3) the D. simulans FRT proteome exhibits limited postmating changes irrespective of whether females mate with conspecific or heterospecific males, suggesting an active female role in mediating reproductive interactions. Our study suggests that divergence in the FRT extracellular environment and postmating response contribute to previously described patterns of postmating-prezygotic isolation and the maintenance of species boundaries.
2020-06-25 | PXD017708 | Pride
Project description:Drosophila dunni species group sequencing and assembly
| PRJNA661260 | ENA
Project description:Reproductive isolation is an intrinsic aspect of species formation. For that reason, the identification of the precise isolating traits, and the rates at which they evolve, is crucial to understanding how species originate and persist. Previous work has measured the rates of evolution of prezygotic and postzygotic barriers to gene flow, yet no systematic analysis has studied the rates of evolution of postmating-prezygotic (PMPZ) barriers. We measured the magnitude of two barriers to gene flow that act after mating occurs but before fertilization. We also measured the magnitude of a premating barrier (female mating rate in nonchoice experiments) and two postzygotic barriers (hybrid inviability and hybrid sterility) for all pairwise crosses of all nine known extant species within the melanogaster subgroup. Our results indicate that PMPZ isolation evolves faster than hybrid inviability but slower than premating isolation. Next, we partition postzygotic isolation into different components and find that, as expected, hybrid sterility evolves faster than hybrid inviability. These results lend support for the hypothesis that, in Drosophila, reproductive isolation mechanisms (RIMs) that act early in reproduction (or in development) tend to evolve faster than those that act later in the reproductive cycle. Finally, we tested whether there was evidence for reinforcing selection at any RIM. We found no evidence for generalized evolution of reproductive isolation via reinforcement which indicates that there is no pervasive evidence of this evolutionary process. Our results indicate that PMPZ RIMs might have important evolutionary consequences in initiating speciation and in the persistence of new species.
| S-EPMC5850467 | biostudies-literature
Project description:Despite holding a central role for fertilisation success, reproductive traits often show elevated rates of evolution and diversification. The rapid evolution of seminal fluid proteins (Sfps) within populations is predicted to cause mis-signalling between the male ejaculate and female reproductive tract between populations resulting in postmating prezygotic (PMPZ) isolation. Crosses between populations of Drosophila montana show PMPZ isolation in the form of reduced fertilisation success in both noncompetitive and competitive contexts. Here we test whether male ejaculate proteins deriving from either the accessory glands or the ejaculatory bulb differ between populations using liquid chromatography tandem mass spectrometry. We find more than 150 differentially abundant proteins between populations which may contribute to PMPZ isolation. These proteins include a number of proteases and peptidases, and several orthologs of D. melanogaster Sfps, all known to mediate fertilisation success and which mimic PMPZ isolation phenotypes. Males of one population typically produced greater quantities of Sfps and the strongest PMPZ isolation occurs in this direction. The accessory glands and ejaculatory bulb have different functions and the ejaculatory bulb contributes more to population differences than the accessory glands. Proteins with a secretory signal, but not Sfps, evolve faster than non-secretory proteins although the conservative criteria used to define Sfps may have impaired the ability to identify rapidly evolving proteins. We take advantage of quantitative proteomics data from three Drosophila species to determine shared and unique functional enrichments of Sfps that could be subject to selection between taxa and subsequently mediate PMPZ isolation. Our study provides the first high throughput quantitative proteomic evidence showing divergence of reproductive proteins implicated in the emergence of PMPZ isolation between populations.
2020-12-01 | PXD019634 | Pride
Project description: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 postmating-prezygotic (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.
| S-EPMC3093519 | biostudies-literature
Project description:In many animals, females respond to mating with changes in physiology and behavior that are triggered by molecules transferred by males during mating. In Drosophila melanogaster, proteins in the seminal fluid are responsible for important female postmating responses, including temporal changes in egg production, elevated feeding rates and activity levels, reduced sexual receptivity, and activation of the immune system. It is unclear to what extent these changes are mutually beneficial to females and males or instead represent male manipulation. Here we use an experimental evolution approach in which females are randomly paired with a single male each generation, eliminating any opportunity for competition for mates or mate choice and thereby aligning the evolutionary interests of the sexes. After >150 generations of evolution, males from monogamous populations elicited a weaker postmating stimulation of egg production and activity than males from control populations that evolved with a polygamous mating system. Males from monogamous populations did not differ from males from polygamous populations in their ability to induce refractoriness to remating in females, but they were inferior to polygamous males in sperm competition. Mating-responsive genes in both the female abdomen and head showed a dampened response to mating with males from monogamous populations. Males from monogamous populations also exhibited lower expression of genes encoding seminal fluid proteins, which mediate the female response to mating. Together, these results demonstrate that the female postmating response, and the male molecules involved in eliciting this response, are shaped by ongoing sexual conflict.
| S-EPMC6486729 | biostudies-literature
Project description: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 with promiscuous mating systems, traits involved in postcopulatory interactions are expected to evolve rapidly, potentially leading to postmating-prezygotic (PMPZ) reproductive isolation between diverging populations. Here, we use a novel study design to investigate the postmating transcriptional response of Drosophila mojavensis female reproductive tracts following copulation with either conspecific or heterospecific (D. arizonae) males at three time points postmating. Relatively few genes (15 total) were transcriptionally 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 downregulated 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, for the first time, the transfer of male mRNA transcripts to females during copulation. These included transcripts from male accessory-gland proteins (ACPs), a finding with potentially broad implications for understanding postcopulatory molecular interactions between the sexes. Dataset from Postmating transcriptional changes in reproductive tracts of con- and heterospecifically-mated Drosophila mojavensis females Bono, JM, Matzkin,LM, Kelleher, ES, and Markow, MA, Proceedings of the National Academy of Sciences, USA.
2012-01-01 | GSE27454 | GEO