Evolutionary history of inshore oceanic island land snails diversified in shell colour

Abstract

AimOceanic islands provide an excellent opportunity to study the mode and tempo of phenotypic evolution of terrestrial organisms. Many studies have focused on oceanic islands far from the mainland. Oceanic islands near the mainland may provide distinct perspectives on phenotypic evolution, but a comprehensive understanding is still lacking. To address this gap, this study aimed to reveal when a land snail species inhabiting a volcanic archipelago within 40 km of the mainland diverged and how their shell colours evolved.LocationSouthern Izu Peninsula and five Izu Islands (Oshima, Toshima, Niijima, Shikine and Kozu), Japan.Taxon Euhadra peliomphala simodae. MethodsDouble‐digest restriction site‐associated DNA sequencing (ddRAD‐seq) was conducted using 117 individual snails. Molecular phylogenetic and population genomic analyses were performed, including approximation Bayesian computation (ABC). We then examined whether the island area, elevation, distance from the surrounding landmasses and historical event (bottleneck) explain the shell colour diversity on each island using a phylogenetic generalised linear mixed model (PGLMM).ResultsSnails could be genetically categorised according to the island they inhabited, and on Niijima, their genetic structure was further divided within the island. The divergence times among the extant populations of the snail dated back to 2.1 million years ago (Ma), which is older than that of other animals occurring in this region. Additionally, island elevation positively affected shell colour diversity, and populations with similar shell colour profiles were phylogenetically different.Main conclusionsIsland land snails diversified early in the ecosystem of the Izu Islands. This suggests that proximity to the mainland, immobility and the physiological tolerance of passive dispersal in land snails were the main causes of early diversification. Moreover, our study proposes that environments covarying with elevation would determine shell colour diversity on each island through natural selection.

Overcoming the congenitally disadvantageous mutation through adaptation to environmental UV exposure in land snails

“…Eventually, dark snails might dominate in high-elevation areas because high UV radiation increases the total fitness advantage of dark snails while decreasing the fitness of white snails. In Oshima, which has a maximum elevation of 758 m and is the highest among the islands inhabited by this snail species, the frequency of shell colour was biased toward the dark across the island [15]. Islands with high elevation showed diverse shell colour [15]; this could be attributed to the heterogeneity in UV radiation intensity.…”

“…Our study used Euhadra peliomphala simodae , a snail species inhabiting the southern part of the Izu Peninsula and the five Izu Islands in Japan (electronic supplementary material, figure S1). Their shells exhibit colour polymorphism and can be classified into dark and bright [15,16]. The disruptive selection affects the colours of island populations, resulting in two different colours having similar survival rates [15,17,18].…”

“…Their shells exhibit colour polymorphism and can be classified into dark and bright [15,16]. The disruptive selection affects the colours of island populations, resulting in two different colours having similar survival rates [15,17,18]. One of the causes of the selection is the co-variation of environmental factors with elevation; however, predation from mammal and avian predators does not directly impact it [15,18].…”

“…The disruptive selection affects the colours of island populations, resulting in two different colours having similar survival rates [15,17,18]. One of the causes of the selection is the co-variation of environmental factors with elevation; however, predation from mammal and avian predators does not directly impact it [15,18]. Therefore, thermoregulation is applicable, whereas camouflage is not.…”

“…Moreover, we analysed whether adaptation to a specific environment contributed to overcoming the congenital fitness disadvantages associated with a specific colour. Based on a previous study [15], we focussed on two external environmental variables that co-varied with elevation. We initially focussed on temperature because the shell colour in some snails serves as a thermoregulatory mechanism [14,19].…”