Premating isolation prevents interspecies mating between two species who can still produce fertilizable hybrids (Sato and Yamamoto, 2020). The model species D. melanogaster and D. simulans were isolated about 1.4 million years ago (Zile et al., 2020). The interspecific mating merely happened in laboratory conditions mainly because of the difference of their sex pheromones. They are well studied at multiple levels including genome, sensillum and neural system, and thus serves as a suitable model to study premating reproductive isolation.
The chemical analysis of cuticular hydrocarbons showed that D. melanogaster female produces 7,11-HD while D. melanogaster male and D. simulans (both sexes) produces 7-T (Jallon and David 1987). A male-male mating experiment showed that 7-T inhibits male homosexual courtship in D. melanogaster (Lacaille et al. 2007). Furthermore, a pheromone perfuming experiment found that D. melanogaster male courted on the 7,11-HD perfumed D. simulans female while D. simulans male didn’t. Instead, perfuming 7-T on D. melanogaster female induces the mating of D. simulans male (Billeter et al. 2009).
How do those sex pheromone chemicals affect the mating behavior of males? The studies on the sex pheromone receptors of these two species showed us that: In D. melanogaster, the ion channels coded by ppk23, ppk25 and ppk29 senses 7,11-HD and promote mating behaviors (Thistle et al. 2012: ppk23 and ppk29; Vijayan et al. 2014: ppk25), while a gustatory receptor Gr32a senses 7-T and inhibits mating behaviors (Fan et al. 2013). In D. simulans, ppk25 still promotes mating while Gr32a has no effect on mating behaviors but has responses to bitter tastes (Ahmed et al. 2019), and ppk23 conserves sensory responses to 7,11-HD (Seeholzer et al. 2018).
However, those studies revealed that 7,11-HD attracts D. melanogaster male to interspecific mating but repels D. simulans male from conspecific mating. Why do they behave so differently towards 7,11-HD without a significant difference in the receptor level? A study on the central nervous circuits found a change in their signalling balance of excitation and inhibition onto courtship-promoting neurons. It showed that both of them can sense 7,11-HD, but it results in excitation in D. melanogaster and inhibition in D. simulans to P1 neurons that trigger the courtship behavior (Seeholzer et al. 2018).
In conclusion, the premating reproductive isolation of D. melanogaster and D. simulans is mainly based on the difference of their sex pheromone production and perception. Furthermore, the main difference of their pheromone perception was not on the receptor level, but on the central circuit level. However, the question why 7-T induces contrasting behaviors to these two species is still unclear. I expect additional research at the central circuit level can reveal it in the future.
References
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