Abstract
The ecological theory of island biogeography suggests that mainland populations should be more genetically divergent from those on large and distant islands rather than from those on small and close islets. Some island populations do not evolve in a linear way, but the process of divergence occurs more rapidly because they undergo a series of phenotypic changes, jointly known as the Island Syndrome. A special case is Reversed Island Syndrome (RIS), in which populations show drastic phenotypic changes both in body shape, skin colouration, age of sexual maturity, aggressiveness, and food intake rates. The populations showing the RIS were observed on islets nearby mainland and recently raised, and for this they are useful models to study the occurrence of rapid evolutionary change. We investigated the timing and mode of evolution of lizard populations adapted through selection on small islets. For our analyses, we used an ad hoc model system of three populations: wild-type lizards from the mainland and insular lizards from a big island (Capri, Italy), both Podarcis siculus siculus not affected by the syndrome, and a lizard population from islet (Scopolo) undergoing the RIS (called P. s. coerulea because of their melanism). The split time of the big (Capri) and small (Scopolo) islands was determined using geological events, like sea-level rises. To infer molecular evolution, we compared five complete mitochondrial genomes for each population to reconstruct the phylogeography and estimate the divergence time between island and mainland lizards. We found a lower mitochondrial mutation rate in Scopolo lizards despite the phenotypic changes achieved in approximately 8,000 years. Furthermore, transcriptome analyses showed significant differential gene expression between islet and mainland lizard populations, suggesting the key role of plasticity in these unpredictable environments.
Highlights
Island evolution and syndromesIsland populations have provided insights on evolutionary processes such as species radiations [1] and the generation of evolutionary novelties [2]
Individual organisms can mitigate the effects of environmental variations in two ways to weaken the selection pressure in a short time: they can move to a new site according to the habitat tracking hypothesis [59] or modulate the activity of some genes to trigger phenotypic changes
Habitat tracking represents a major explanation for morphological stasis, which is one of the pillars of the theory of punctuated equilibrium [60,61]
Summary
Island populations have provided insights on evolutionary processes such as species radiations [1] and the generation of evolutionary novelties [2]. The adaptations developed by Scopolo population (under RIS) were the result of changes in gene expression [22,24,25] This hypothesis implies that after mutational events, genes underwent the DNA fixation process in the island population, as suggested by observing mtGenome, with a simultaneous transcriptome plasticity which leads to the differential gene expression, in response to selection. The mutation rate found in the population of Scopolo should be significantly slower than in isolated population, but not influenced by very strong adaptations, as under RIS (i.e., Capri) This lower mutation rate observed on the mtGenome of insular populations, such as Scopolo, could lead to an erroneous conclusion about a lower speed of the evolution. It is necessary to take consider that the response to natural selection could result in epigenetic events rather than mutations
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