The roles of geological history and colonization abilities in genetic differentiation between mammalian populations in the Philippine archipelago

Aim To test hypotheses that: (1) late Pleistocene low sea-level shorelines (rather than current shorelines) define patterns of genetic variation among mammals on oceanic Philippine islands; (2) species-specific ecological attributes, especially forest fidelity and vagility, determine the extent to which common genetic patterns are exhibited among a set of species; (3) populations show reduced within-population variation on small, isolated oceanic islands; (4) populations tend to be most highly differentiated on small, isolated islands; and (5) to assess the extent to which patterns of genetic differentiation among multiple species are determined by interactions of ecological traits and geological/geographic conditions. Location The Philippine Islands, a large group of oceanic islands in Southeast (SE) Asia with unusually high levels of endemism among mammals. Methods Starch-gel electrophoresis of protein allozymes of six species of small fruit bats (Chiroptera, Pteropodidae) and one rodent (Rodentia, Muridae). Results Genetic distances between populations within all species are not correlated with distances between present-day shorelines, but are positively correlated with distances between shorelines during the last Pleistocene period of low sea level; relatively little intraspecific variation was found within these ‘Pleistocene islands’. Island area and isolation of oceanic populations have only slight effects on standing genetic variation within populations, but populations on some isolated islands have heightened levels of genetic differentiation, and reduced levels of gene flow, relative to other islands. Species associated with disturbed habitat (all of which fly readily across open habitats) show more genetic variation within populations than species associated with primary rain forest (all of which avoid flying out from beneath forest canopy). Species associated with disturbed habitats, which tend to be widely distributed in SE Asia, also show higher rates of gene flow and less differentiation between populations than species associated with rain forest, which tend to be Philippine endemic species. One rain forest bat has levels of gene flow and heterozygosity similar to the forest-living rodent in our study. Main conclusions The maximum limits of Philippine islands that were reached during Pleistocene periods of low sea level define areas of relative genetic homogeneity, whereas even narrow sea channels between adjacent but permanently isolated oceanic islands are associated with most genetic variation within the species. Moreover, the distance between ‘Pleistocene islands’ is correlated with the extent of genetic distances within species. The structure of genetic variation is strongly influenced by the ecology of the species, predominantly as a result of their varying levels of vagility and ability to tolerate open (non-forested) habitat. Readily available information on ecology (habitat association and vagility) and geological circumstances (presence or absence of Pleistocene land-bridges between islands, and distance between oceanic islands during periods of low sea level) are combined to produce a simple predictive model of likely patterns of genetic differentiation (and hence speciation) among these mammals, and probably among other organisms, in oceanic archipelagos.