Reinforcement of Gametic Isolation in Drosophila

D. santomea and D. yakuba provide an example of reinforcement for a postmating-prezygotic trait in an organism that has internal fertilization. This work shows that reinforcement of barriers other than sexual and other forms of premating isolation is possible.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.Author Summary: What stops newly formed species from interbreeding? Answering this question is fundamental to our understanding of speciation. One mechanism is that where such would-be species meet, the barriers against interbreeding are reinforced by natural selection (e.g., leading to greater mate discrimination). On the slopes of the African island of São Tomé, Drosophila yakuba and its sister species D. santomea hybridize within a well-demarcated hybrid zone. I found that D. yakuba females from within this zone, but not from outside it, show an increase in gametic isolation from males of D. santomea, such that before fertilization, the females deplete sperm from D. santomea males faster than from conspecific males. Consequently, there are fewer progeny produced from interspecific matings. By experimentally evolving the populations, I also show that such postmating isolation can rapidly evolve. Natural selection, therefore, has promoted the evolution of stronger interspecific genetic barriers that act after mating but before fertilization. D. santomea and D. yakuba, then, appear to represent an example of reinforcement for a postmating-prezygotic trait in an organism that has internal fertilization. This work shows that reinforcement of barriers other than sexual and other forms of premating isolation is possible. This also suggests that there are many “cryptic” barriers to gene flow that might be increased by natural selection in areas where species overlap and hybridize.