A time-calibrated phylogenetic approach to assessing the phylogeography, colonization history and phenotypic evolution of snakes in the Japanese Izu Islands

Abstract

Aim We infer the biogeography and colonization history of a dispersal-limited terrestrial vertebrate, the Japanese four-lined ratsnake (Elaphe quadrivirgata), to reveal the number of times mainland populations have invaded the Izu Archipelago of Japan, the mainland sources of these colonists, and the timescale of colonization. We compare these results with those of past studies in an attempt to uncover general biogeographical patterns. Moreover, we briefly examine the significance of colonization history when evaluating the evolution of body size and melanism of the Izu Island E. quadrivirgata populations.Location The Izu Islands (Oshima, Toshima, Niijima, Shikine, Kozu, Tadanae and Mikura), a volcanic archipelago off the Pacific coast of central Japan.Methods We obtained DNA sequences of the mitochondrial cytochrome b gene (1117 base pairs) from 373 individual snakes sampled from seven of the Izu Islands and 25 mainland localities. We employed partitioned Bayesian phylogenetic analyses assuming a relaxed molecular clock to estimate phylogenetic relationships among extant haplotypes and to give an explicit temporal scale to the timing of clade divergence, colonization history and tempo of body-size evolution. Moreover, we employed model-based biogeographical analysis to calculate the minimum number of times E. quadrivirgata colonized the Izu Islands.Results We found evidence that three separate regions of the Izu Archipelago have been colonized independently from mainland ancestors within the past 0.58-0.20 Ma. The Izu Peninsula plus Oshima and Mikura were both colonized independently from lineages inhabiting eastern mainland Japan. The Toshima, Niijima, Shikine, Kozu and Tadanae populations all derive from a single colonization from western mainland Japan. Oshima has been subject to three or possibly four colonizations.Main conclusions These results support the hypothesis that the extreme body-size disparity among island populations of this ratsnake evolved in situ. Moreover, the fact that the dwarf, melanistic population inhabiting Oshima descends from multiple mainland colonization events is evidence of an extremely strong natural selection pressure resulting in the rapid evolution of this unique morphology. These results contrast with theoretical predictions that natural selection pressures should play a decreased role on islands close to the mainland and/or subject to frequent or recent immigration.

Divergence before and after the isolation of islands: Phylogeography of the Bradybaena land snails on the Ryukyu Islands of Japan

“…The Izu Islands were probably formed within the past million years as oceanic islands (Kaneko, Issiki, & Zashu, ). This is consistent with our results as well as the other evolutionary patterns of the endemic organisms of the islands (Kuriyama, Brandley, Katayama, Mori, et al., ). Subclades 4–6 from clade F appear to have migrated from south to north, because the ancestral lineages tend to be distributed in the areas of lower latitude.…”

Tracing the origins of widespread highland species: a case of Neogene diversification across the Mexican sierras in an endemic lizard

“…These gene regions have been previously shown to be informative at different levels of divergence within lizards (Leaché & Mulcahy, 2007; Lindell, Méndez‐de la Cruz & Murphy, 2008). Although it has been demonstrated that single locus genetic studies have some limitations (Edwards & Bensch, 2009), mtDNA nonetheless remains useful in exploring geographical relationships among closely‐related species (Pyron & Burbrink, 2009; Daza, Castoe & Parkinson, 2010; Kuriyama et al ., 2011). Primer sequences for ATPase were specifically designed for this project (C2LF4, 5′‐CAATGCTCAGARATYTGYGG‐3′; C3LR, 5′‐GCGTGTGYTTGGTGGGTCAT‐3′), and required an annealing temperature of 50 °C.…”

Relying on a Single Anuran Species: Feeding Ecology of a Snake Community on Kinkasan Island, Miyagi Prefecture, Japan

“…tigrinus (Tanaka and Ota, 2002). Body size changes of snakes on island populations are generally considered to be associated with a diet alteration related to prey type, prey size, and/or the abundance of prey (e.g., Hasegawa and Moriguchi, 1989; Boback, 2003;Hasegawa and Mori, 2008 Fukada, 1992;Kadowaki, 1996;Kuriyama et al, 2011;Tanaka, 2011;Tanaka and Mori, 2011), Rh. tigrinus (mean SVL, 563-607 mm for males, 630-785 mm for females ;Fukada, 1992;Kadowaki, 1996; also see Moriguchi [1985] for frequency distribution of SVL), and G. blomhoffii (mean SVL, 411-461 mm for males, 422-512 mm for females ;Fukada, 1992;Kadowaki, 1996;Yomeishu Seizo Co. Ltd., 1999), but suggests possible dwarfism in El.…”