The impact of different reproductive barriers on species or population isolation may vary in different stages of speciation depending on evolutionary forces acting within species and through species’ interactions. Genetic incompatibilities between interacting species are expected to reinforce prezygotic barriers in sympatric populations and lead to cascade reinforcement between conspecific populations living within and outside the areas of sympatry. We tested these predictions and studied whether and how the strength and target of reinforcement between Drosophila montana and Drosophila flavomontana vary between sympatric populations with different histories and species abundances. All barriers between D. montana females and D. flavomontana males were nearly complete, while in the reciprocal cross strong postzygotic isolation was accompanied by prezygotic barriers whose strength varied according to population composition. Sexual isolation between D. flavomontana females and D. montana males was increased in long‐established sympatric populations, where D. flavomontana is abundant, while postmating prezygotic (PMPZ) barriers were stronger in populations where this species is a new invader and still rare and where female discrimination against heterospecific males was lower. Strengthening of sexual and PMPZ barriers in this cross also induced cascade reinforcement of respective barriers between D. flavomontana populations, which is a classic signature of reinforcement process.
The incidence of reproductive diapause is a critical aspect of life history in overwintering insects from temperate regions. Much has been learned about the timing, physiology and genetics of diapause in a range of insects, but how the multiple changes involved in this and other photoperiodically regulated traits are interrelated is not well understood. We performed quasinatural selection on reproduction under short photoperiods in a northern fly species, Drosophila montana, to trace the effects of photoperiodic selection on traits regulated by the photoperiodic timer and/or by a circadian clock system. Selection changed several traits associated with reproductive diapause, including the critical day length for diapause (CDL), the frequency of diapausing females under photoperiods that deviate from daily 24 h cycles and cold tolerance, towards the phenotypes typical of lower latitudes. However, selection had no effect on the period of free-running locomotor activity rhythm regulated by the circadian clock in fly brain. At a genomic level, selection induced extensive divergence from the control line in 16 gene clusters involved in signal transduction, membrane properties, immunologlobulins and development. These changes resembled those detected between latitudinally divergent D. montana populations in the wild and involved SNP divergence associated with several genes linked with diapause induction. Overall, our study shows that photoperiodic selection for reproduction under short photoperiods affects diapause-associated traits without disrupting the central clock network generating circadian rhythms in fly locomotor activity.
Selection experiments offer an efficient way to study the evolvability of traits that play an important role in insects' reproduction and/or survival and to trace correlations and trade-offs between them. We have exercised bi-directional selection on Drosophila montana flies' preadult development time under constant light and temperature conditions for 10 generations and traced the indirect effects of this selection on females' diapause induction under different day lengths, as well as on the body weight and cold tolerance of both sexes. Overall, selection was successful towards slow, but not towards fast development. However, all fast selection line replicates showed at the end of selection increased variance in females' photoperiodic diapause response and about one hour increase in the critical day (CDL), where more than 50 % of emerging females enter diapause. Indirect effects of selection on flies' body weight and cold-tolerance were less clear, as the flies of the slow selection line were significantly heavier and less cold-tolerant than the control line flies after five generations of selection, but lighter and more cold-tolerant at the end of selection. Changes in females' diapause induction resulting from selection for fast development could be due to common metabolic pathways underlying these traits, collaboration of circadian clock and photoperiodic timer and / or by the interaction between the endocrine and circadian systems.
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 ...
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