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Reinforcement of gametic isolation in Drosophila.

ABSTRACT: Reinforcement, a process by which natural selection increases reproductive isolation between populations, has been suggested to be an important force in the formation of new species. However, all existing cases of reinforcement involve an increase in mate discrimination between species. Here, I report the first case of reinforcement of postmating prezygotic isolation (i.e., barriers that act after mating but before fertilization) in animals. On the slopes of the African island of São Tomé, Drosophila yakuba and its endemic sister species D. santomea hybridize within a well-demarcated hybrid zone. I find that D. yakuba females from within this zone, but not from outside it, show an increase in gametic isolation from males of D. santomea, an apparent result of natural selection acting to reduce maladaptive hybridization between species. To determine whether such a barrier could evolve under laboratory conditions, I exposed D. yakuba lines derived from allopatric populations to experimental sympatry with D. santomea, and found that both behavioral and gametic isolation become stronger after only four generations. Reinforcement thus appears to be the best explanation for the heightened gametic isolation seen in sympatry. This appears to be the first example in animals in which natural selection has promoted the evolution of stronger interspecific genetic barriers that act after mating but before fertilization. This suggests that many other genetic barriers between species have been increased by natural selection but have been overlooked because they are difficult to study.

SUBMITTER: Matute DR

PROVIDER: S-EPMC2843595 | biostudies-literature | 2010 Mar

REPOSITORIES: biostudies-literature

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Reinforcement of gametic isolation in Drosophila.

Matute Daniel R DR

PLoS biology 20100323 3

Reinforcement, a process by which natural selection increases reproductive isolation between populations, has been suggested to be an important force in the formation of new species. However, all existing cases of reinforcement involve an increase in mate discrimination between species. Here, I report the first case of reinforcement of postmating prezygotic isolation (i.e., barriers that act after mating but before fertilization) in animals. On the slopes of the African island of São Tomé, Droso ...[more]

PMID: 20351771

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Project description:Reinforcement refers to the evolution of increased mating discrimination against heterospecific individuals in zones of geographic overlap and can be considered a final stage in the speciation process. One the factors that may affect reinforcement is the degree to which hybrid matings result in the permanent loss of genes from a species' gene pool. Matings between females of Drosophila subquinaria and males of D. recens result in high levels of offspring mortality, due to interspecific cytoplasmic incompatibility caused by Wolbachia infection of D. recens. Such hybrid inviability is not manifested in matings between D. recens females and D. subquinaria males. Here we ask whether the asymmetrical hybrid inviability is associated with a corresponding asymmetry in the level of reinforcement. The geographic ranges of D. recens and D. subquinaria were found to overlap across a broad belt of boreal forest in central Canada. Females of D. subquinaria from the zone of sympatry exhibit much stronger levels of discrimination against males of D. recens than do females from allopatric populations. In contrast, such reproductive character displacement is not evident in D. recens, consistent with the expected effects of unidirectional cytoplasmic incompatibility. Furthermore, there is substantial behavioral isolation within D. subquinaria, because females from populations sympatric with D. recens discriminate against allopatric conspecific males, whereas females from populations allopatric with D. recens show no discrimination against any conspecific males. Patterns of general genetic differentiation among populations are not consistent with patterns of behavioral discrimination, which suggests that the behavioral isolation within D. subquinaria results from selection against mating with Wolbachia-infected D. recens. Interspecific cytoplasmic incompatibility may contribute not only to post-mating isolation, an effect already widely recognized, but also to reinforcement, particularly in the uninfected species. The resulting reproductive character displacement not only increases behavioral isolation from the Wolbachia-infected species, but may also lead to behavioral isolation between populations of the uninfected species. Given the widespread occurrence of Wolbachia among insects, it thus appears that there are multiple ways by which these endosymbionts may directly and indirectly contribute to reproductive isolation and speciation.

Project description:BackgroundDuring the speciation process several types of isolating barriers can arise that limit gene flow between diverging populations. Studying recently isolated species can inform our understanding of how and when these barriers arise, and which barriers may be most important to limiting gene flow. Here we focus on Drosophila suboccidentalis and D. occidentalis, which are closely related mushroom-feeding species that inhabit western North America and are not known to overlap in geographic range. We investigate patterns of reproductive isolation between these species, including premating, postmating prezygotic, and postzygotic barriers to gene flow.ResultsUsing flies that originate from a single population of each species, we find that the strength of premating sexual isolation between these species is asymmetric: while D. occidentalis females mate with D. suboccidentalis males at a reduced but moderate rate, D. suboccidentalis females discriminate strongly against mating with D. occidentalis males. Female hybrids will mate at high rates with males of either species, indicating that this discrimination has a recessive genetic basis. Hybrid males are accepted by females of both species. We do not find evidence for postmating prezygotic or postzygotic isolating barriers, as females use the sperm of heterospecific males and both male and female hybrids are fully fertile.ConclusionsPremating isolation is substantial but incomplete, and appears to be the primary form of reproductive isolation between these species. If these species do hybridize, the lack of postzygotic barriers may allow for gene flow between them. Given that these species are recently diverged and are not known to be sympatric, the level of premating isolation is relatively strong given the lack of intrinsic postzygotic isolation. Further work is necessary to characterize the geographic and genetic variation in reproductive isolating barriers, as well as to determine the factors that drive reproductive isolation and the consequences that isolating barriers as well as geographic isolation have had on patterns of gene flow between these species.

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Reinforcement of gametic isolation in Drosophila.

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Reinforcement of gametic isolation in Drosophila.

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