Two different adaptive speciation mechanisms operate during adaptation to a novel hot environment

Abstract

Ambient temperature is one major ecological factor driving adaptation in natural populations, but its impact on the emergence of new species is not yet clear. Here, we explored the evolution of reproductive isolation during temperature adaptation by exposing 10 replicate Drosophila simulans populations to a hot temperature regime. Within less than 200 generations, both pre- and post-mating reproductive isolation evolved. The altered lipid metabolism of evolved flies also affected the cuticular hydrocarbon (CHCs) profiles. Different CHC profiles could explain the emerged assortative mating between ancestral and evolved populations. Hence, we identified the hallmark of ecological speciation driven by temperature adaptation. While this pre-mating isolation occurred only between ancestral and evolved replicate populations, post-mating reproductive isolation was observed among evolved replicate populations. We propose that epistatic interactions of reproduction-related genes between males and females resulted in adaptive co-evolution. Incompatibilities between different gene combinations favored in each replicate could explain the observed post-mating reproductive isolation. We anticipate that this “mutation-order-like speciation” from standing genetic variation, a new speciation process, is widespread in nature when highly polygenic traits are involved in adaptation.

Non‐additive effects between genotypes: Implications for competitive fitness assays

“…We used an inbred reference strain with white eyes (w501) in pairwise competition with multiple polymorphic populations, which evolved in different temperature regimes (Table 1). Since our focal populations show pre‐mating reproductive isolation (Hsu et al., 2023), we did not include sexual competition in our fitness assays. Our fitness estimates combined the fitness components fecundity and viability.…”

“…Furthermore, the CHC composition has evolved during adaptation to a hot fluctuating environment (Hsu et al, 2023). Hence, it is conceivable that larvae cannibalize preferentially genetically distinct larvae.…”

“…Larvae have been shown to distinguish between genetically distinct eggs and preferentially cannibalize eggs with different ancestry (Narasimha et al., 2019). Furthermore, the CHC composition has evolved during adaptation to a hot fluctuating environment (Hsu et al., 2023). Hence, it is conceivable that larvae cannibalize preferentially genetically distinct larvae.…”

“…Since we were interested to obtain fitness estimates that include most aspects of the life cycle, we allowed 100 mated females to lay eggs for 48 h. Hence, our fitness assays include fecundity and viability. We did not include sexual competition in our fitness assays to exclude confounding effects arising from pre-mating reproductive isolation which was detected in some of the focal populations (Hsu et al, 2023). The interpretation of fitness can differ when sexual competition is not included; therefore, it is in general advisable to measure fitness across the entire life cycle of an organism (Prout, 1965(Prout, , 1971.…”