Snake and Bird Predation Drive the Repeated Convergent Evolution of Correlated Life History Traits and Phenotype in the Izu Island Scincid Lizard (Plestiodon latiscutatus)

Abstract

Predation may create strong natural selection pressure on the phenotype and life history characteristics of prey species. The Izu scincid lizards (Plestiodon latiscutatus) that inhabit the four Japanese Izu Islands with only bird predators are drab brown, mature later, lay small clutches of large eggs, and hatch large neonates. In contrast, skinks on seven islands with both snake and bird predators are conspicuously colored, mature early, lay large clutches of small eggs, and hatch small neonates. We test the hypothesis that these suites of traits have evolved independently on each island via natural selection pressures from one of two predator regimes – birds-only and birds + snakes. Using two mtDNA genes and a nuclear locus, we infer a time-calibrated phylogeny of P. latiscutatus that reveals a basal split between Mikura and all islands south, and Miyake, all islands north, and the Izu Peninsula. Populations inhabiting Miyake, Niijima, Shikine, and Toshima are not monophyletic, suggesting either multiple colonizations or an artifact of incomplete lineage sorting (ILS). We therefore developed novel phylogenetic comparative analyses that assume either a multiple colonization or more restrictive single colonization ILS scenario and found 1) statistically significant support for the of different suites of phenotypic and life history characteristics with the presence of bird-only or bird + snake predator assemblages, and 2) strong phylogenetic support for at least two independent derivations of either the “bird-only” or “snakes + birds” phenotypes regardless of colonization scenario. Finally, our time-calibrated phylogeographic analysis supports the conclusion that the ancestor to modern Izu Island P. latiscutatus dispersed from the mainland to the Izu proto-islands between 3–7.6 million years ago (Ma). These lineages remained present in the area during successive formation of the islands, with one lineage re-colonizing the mainland 0.24-0.7 Ma.

Cellular basis of anti‐predator adaptation in a lizard with autotomizable blue tail against specific predators with different colour vision

“…Classical decoy hypothesis predict that increased bird predation promote evolution of blue tail (Bateman et al ., ). However, lizards of Hachijokojima, Miyake and Aogashima where the thrush Turdus celaenops , a primary predator on juvenile lizard is abundant (Brandley et al ., ) showed the lowest reflectance of either blue or UV compared to the Kozu and Izu Peninsula populations (Fig. ).…”

“…The proportion of the length of the blue coloured portion to the total tail length was the shortest in Hachijokojima, the medium in Kozu and the longest in Izu Peninsula (Fig. ; Brandley et al ., ). Light reflectance of tail colouration was measured for a total of 15 juvenile lizards younger than 1‐year post‐hatching, with typical juvenile body colouration and unbroken tail [Peninsula, n = 3, snout‐vent length (SVL), ± sd (mm) = 42.7 ± 4.0, TL (tail length) 70.3 ± 8.1; Kozu, n = 7, SVL 46.6 ± 2.4, TL 80.6 ± 4.8; Hachijokojima, n = 5, SVL 46.6 ± 5.9, TL 76.0 ± 10.8].…”

“…). Phylogenetic evidence has shown that either a vivid blue or drab brown tail colouration has independently evolved at least twice in P. latiscutatus , thereby supporting the hypothesis that tail colouration has evolved via strong natural selection (Brandley et al ., ).…”

“…Populations of the Okada's five‐lined skink, Plestiodon latiscutatus (formerly P. okadae ; Okamoto et al ., ) are notable for the geographical variation in juvenile tail colouration on the Japanese Izu Peninsula the major Izu Islands; moreover, these different phenotypes are associated with the islands' predator assemblages that vary in the relative abundance of weasels, snakes, and birds (Fig. ; Brandley, Kuriyama & Hasegawa, ). In the northern Izu Islands and Izu Peninsula (Fig.…”

Oceanic island biogeography: Nomothetic science of the anecdotal

“…Life history shifts (e.g. Tamarin 1978, Adler and Levins 1994, Blondel 2000, Raia et al 2010, Pafilis et al 2011, Brandley et al 2014) and density increases (e.g. Crowell 1962, Case 1975, Rodda and DeanBradley 2002, Novosolov et al 2016) similarly seem to occur on all island types.…”