Ecological gradients drive insect wing loss and speciation: The role of the alpine treeline

Abstract

Alpine ecosystems are frequently characterized by an abundance of wing‐reduced insect species, but the drivers of this biodiversity remain poorly understood. Insect wing reduction in these environments has variously been attributed to altitude, temperature, isolation, habitat stability or decreased habitat size. We used fine‐scale ecotypic and genomic analyses, along with broad‐scale distributional analyses of ecotypes, to unravel the ecological drivers of wing reduction in the wing‐dimorphic stonefly Zelandoperla fenestrata complex. Altitudinal transects within populations revealed dramatic wing reduction over very fine spatial scales, tightly linked to the alpine treeline. Broad biogeographical analyses confirm that the treeline has a much stronger effect on these ecotype distributions than altitude per se. Molecular analyses revealed parallel genomic divergence between vestigial‐winged (high altitude) and full‐winged (low altitude) ecotypes across distinct streams. These data thus highlight the role of the alpine treeline as a key driver of rapid speciation, providing a new model for ecological diversification along exposure gradients.

Dispersal limitation: Evolutionary origins and consequences in arthropods

“…Shifts from above‐ground to subterranean habitats are also associated with evolved dispersal limitation, where traits other than wings are involved in evolutionary change (Juan, Guzik, Damiá, & Cooper, ). Similar to the observations of McCulloch et al (), occupancy of geographically isolated subterranean habitats can also be achieved by repeated and convergent speciation over relatively short spatial scales (e.g., Villacorta, Jaume, Oromí, & Juan, ). This theme of repeated evolution of dispersal limitation along ecological gradients is also seen in islands.…”

“…However, understanding the evolutionary process behind these patterns has been limited. In this issue of Molecular Ecology , McCulloch et al () provide compelling evidence for the evolution of reduced dispersal ability driven by contrasting selection between habitats (above and below the alpine tree line) in the stonefly species Zelandoperla fenestrata (Figure ). They build on earlier work to demonstrate parallel evolution of flightless ecotypes from a common flighted ancestor in freshwater streams.…”

“…By generating large scale genomic data at a fine spatial scale, McCulloch et al () have been able to demonstrate clear evidence for repeated genomic divergence from an ancestral fully‐winged ecotype of Z. fenestrata giving rise to vestigial‐winged ecotypes of independent origin. Their data are compatible with an explanation of ecological speciation of wingless alpine insects along exposure gradients, specifically associated with the treeline, which presumably acts to enhance the steepness of the selection gradient.…”

“…The spatial scale of convergent evolution (sensu Losos, ) of dispersal limitation described for Z. fenestrata is surprising, and raises the question of how general this phenomena might be in nature, with McCulloch et al () suggesting that at least in Z. fenestrata it may be very frequent. Suzuki et al () present phylogenetic data for Japanese scorpionflies that also reveal repeated evolution of dispersal limitation in Panorpodes paradoxus , but in contrast to Z. fenestrata , P. paradoxus presents only limited wing reduction.…”

“…Evolution toward reduced dispersal ability has been the subject of much speculation at the macroevolutionary and macroecological scales, specifically with regard to flight. McCulloch et al () provide much needed insight on the microevolutionary path toward reduced dispersal ability. While dispersal limitation is typically addressed in terms of flight ability, evolutionary transitions from good disperser to poor disperser are not limited to winged species.…”