Reinforcement targets sexual or postmating prezygotic reproductive barriers depending on species abundance and population history

Abstract

21The impact of different reproductive barriers on species or population isolation may vary in different 22 stages of speciation depending on evolutionary forces acting within species and through species' 23 interactions. Genetic incompatibilities between interacting species are expected to reinforce 24 prezygotic barriers in sympatric populations and create character displacement between conspecific 25 populations living within and outside the area of sympatry. The outcome of reinforcement has been 26 suggested to be affected by the strength of postzygotic barriers, the history of species coexistence, 27 and the impact of species abundancies on females' discrimination against heterospecific males. We 28 tested these predictions in Drosophila montana and Drosophila flavomontana populations from 29 different geographic regimes. All barriers between D. montana females and D. flavomontana males 30 were extremely strong, while in the reciprocal cross postzygotic isolation was less effective and the 31 target of reinforcement varied according to population type. In long-established sympatric 32 populations, where D. flavomontana is abundant, reinforcement targeted sexual isolation, and in 33 populations, where this species is a new invader and rare, reinforcement targeted postmating 34 prezygotic barriers. Reinforcement of these barriers also created respective barriers between different 35 D. flavomontana populations. These findings show that interspecies interactions have far-reaching 36 effects on strengthening species barriers and promoting speciation.37 65 vary between the interacting species, and different sensory modalities and courtship cues used in 66 courtship and mating may differ between closely-related species (Gleason et al. 2012; Giglio and 67 Dyer 2013; Colyott et al. 2016). Reinforcement enhances female discrimination against 68 heterospecific males in sympatric populations and increases their discrimination towards conspecific 69 males, and thus sympatric females may reject allopatric males as mates. The converse (i.e., allopatric 70 females with sympatric males) need not be true (Noor 1999; Hoskin et al. 2005; Jaenike et al. 2006; 71 Bewick and Dyer 2014). Most of the identified PMPZ barriers, including incompatibilities in the 72 transfer, storage and use of heterospecific sperm, involve discordant interactions between gametes or 73 between the female reproductive tract and male seminal fluids, and they can function after a single 74 mating (Howard 1999; Wirtz 1999; Price et al. 2001; Howard et al. 2009). Even though postmating 75 interactions can have important fitness consequences for both sexes, reinforcement of PMPZ barriers 76 in insect species has been reported only between D. yakuba and D. santomea (Matute 2010) and 77 between D. pseudoobscura and D. persimilis (Castillo and Moyle 2017). 78 Reinforcement is most likely when species hybridization is common and its costs are high, and when 79 the opposing forces of gene flow and recombination are weak (e.g. Servedio and Noor 2003; Coyne 80 ...