Direction and history of the adaptive evolution in shell colour on island land snails

概要

Nature is often complex,” as B.C. Clark stated in his 1979 paper, and evolution is a complex process that involves both deterministic and stochastic processes. Thus, how organisms have evolved is the most puzzling yet interesting subject. Many researchers have tried to solve this problem for a long time. Moreover, understanding this topic leads to the elucidation of population dynamics, community formation, and ecosystem functions. It can help to predict the future course of evolution itself. Hence, elucidating the direction of evolution should play a central role in evolutionary biology in a rapidly changing environment. However, the course of evolution is still unpredictable.

Land snails are traditional material for studying evolutionary biology. The knowledge of their evolution has also provided abundant insight into the evolutionary pattern itself, as well as community assembly and ecological function. My PhD thesis focused on the shell colour of the land snail, Euhadra peliomphala simodae, on the Izu Peninsula and Izu Islands. This snail on the Izu Peninsula is ancestral, and they migrated into the Izu Islands. Island populations have diversified in shell colour after the migration. In contrast, island populations vary in their shell colour variability. Therefore, understanding the tempo and mode of shell colour diversification on each island can provide insight into the evolution of the phenotype. However, it is unclear when and how their shell colour diversified. Hence, I studied them using ecological, experimental, and genetic analysis to clarify the direction and history of adaptive evolution on shell colour.

In chapter 1, I verified the effect of disruptive selection on shell colour polymorphism in the Japanese land snail Euhadra peliomphala simodae. I conducted field surveys on an oceanic island of the Izu Islands, with black, yellow and intermediate-coloured snails, capturing and marking approximately 1,800 individual snails and monitoring their survival over 18 months. Bayesian estimates then showed lower survival rates for the juvenile intermediate-coloured snails than for juvenile black and yellow snails, implying disruptive selection associated with shell colour. I suggest this disruptive selection may result in a pattern of adaptive radiation in land snails.

In chapter 2, I demonstrated how the shell colour of the Japanese land snail Euhadra peliomphala simodae has diversified via a shift in natural selection due to ecological release after migration from the mainland to an island. I used trail-camera traps to identify the cause of natural selection on both the mainland and the island. I also conducted a mark-recapture experiment while collecting microhabitat use data. In total, I captured and marked around 1,700 snails on the mainland. Some of them were preyed upon by an unknown predator. The trail-camera traps showed that the predator is the large Japanese field mouse Apodemus speciosus, and the predatory frequency was higher on the mainland than on the island. Microhabitat use on the island was more extensive than on the mainland, with snails using both ground and arboreal. A Bayesian estimation showed that the stabilising selection on shell colour came from factors other than predation. These results suggest that the course of natural selection was modified due to ecological release after migration from the mainland, explaining one cause of the phenotypic diversification.

In chapter 3, I conducted the morphological and genetic analysis and crossing experiment using this snail to detect the mechanisms of the source and maintain colour polymorphism. I found no difference in the shell and genital morphology and genetic structure between shell colours. In concordance with these results, snails crossed between inter-colours. Then, inter-coloured crossing produced intermediate-coloured offspring. The survival rate of them showed that the same as the progeny of yellow- coloured crossing. These results implied no reproductive isolation, and inter-coloured crossing is the source of polymorphism. I also suggested that an island-specific environment contributes to the natural selection for maintaining polymorphism.

In chapter 4, I conducted molecular phylogenetic and population genomic analysis with 117 individual snails sampled from the Izu Peninsula and five Izu Islands using the double digest restricted-site associated DNA sequencing (ddRAD-seq). I found that snails could be divided into each island. The divergence time into each population was concordant with the initial formation time from volcanic activity and other organisms. Besides, shell colour variation differed among different islands. This study demonstrated that island land snails diversified early in the ecosystem of the Izu Islands. Moreover, my results supported the hypothesis that island-specific divergent selection determined the shell colour frequency, and some were diversified in parallel. Furthermore, it was suggested that recent volcanic activity induced extreme colour diversity via hybridization.

Finally, I discussed the direction and history of adaptive evolution on shell colour of E. p. simodae. These results support the idea that shell colour in these snails was determined mainly by natural selection from the environment. On the other hand, other deterministic and stochastic processes, such as predation, phylogenetic signals, hybridization, and genetic drift via founder effects, also have directly or indirectly regulated shell colour variations. Thus, the evolution of the phenotype in this species has not been simple, but has proceeded through a complex interplay of island-specific factors.