Cryptic diversity and rapid radiation of Indo-Australasian bent-winged bats (Miniopterus Bonaparte, 1837)

Abstract

Global biodiversity hotspots still contain undocumented vertebrate biodiversity. For mammals, most descriptions of new species now result from the discovery of cryptic forms when surveying new areas, or when resolving taxonomically problematic groups. Progress is restrained not only by the taxonomic impediment, but by gaps in geographic and taxonomic sampling, a legacy of available nomenclature from earlier taxonomy, and the availability of methods that provide sufficient resolution of species boundaries among cryptic taxa. Biodiversity hotspots such as Indo-Australasia, where biogeographic regions have been delineated based on patterns of faunal discontinuity, are ideal settings for investigating the mechanisms that produce the diversification of lineages. A conspicuous example with unresolved taxonomy, difficulty with identifications because of a lack of diagnostic morphological characters, and undescribed cryptic diversity are the bent-winged bats (Miniopteridae: Miniopterus), which have spread from the Palaearctic, through Southeast Asia and Indonesia to Australasia. Across this range it is typical to find more than one size-differentiated species in sympatry, and several species are regarded as having very broad ranges. A comprehensive study has not been attempted for the regional group with modern methods that have resolving power for speciation questions. Of particular interest is how this group diversified and radiated across islands and biogeographic barriers, and whether the overt level of morphological similarity within the group conceals an adaptive process. This study applied a multi-disciplinary approach based on extensive geographic and taxonomic sampling to assess the question What is the level of diversity within Indo- Australasian Miniopterus? The key strategy was to use genome-wide nuclear DNA markers to first identify the major lineages and test species boundaries among putative taxa, and then associate each with a geographic range, a morphological form using 3D geometric and classical morphometrics, and biogeographic history from a time tree derived from a mitochondrial DNA phylogeny and biogeographic analysis. Clear evidence of two distinct regional clades was present, separating the genus into Indo- Australasian and African-European lineages that diverged c. 9.71 mya in the mid-Miocene. One significant implication is that the apparently widespread M. schreibersii does not exist in Indo-Australasia. The ancestor of all Indo-Australasian Miniopterus diverged either within Wallacea, or both Wallacea and Sundaland, spreading eastwards to Australasia and westwards back from Wallacea. Recent rapid radiation of Miniopterus occurred during the late Pliocene to Pleistocene when ancestral forms crossed Huxley’s, Wallace’s and Lydekker’s lines of faunal discontinuity when sea levels were low. The three body size classes identified by Tate (1941) corresponded to four major genetic clades, with the smallest size class consisting of two major clades. Patterns of allometry from quantitative 3D shape analysis also showed four major groups based on skull shape that were concordant with the four major genetic clades, and suggestive of genus-level distinction. Furthermore, 29 distinct genetic lineages were identified, each a putative species. This effectively doubles the number of species identified based on past morphological analyses. Seventeen of those 29 taxa have available names based on previous descriptions and are currently listed species and sub species. The remainder are unnamed, and are either representative of synonymised names or taxa that are completely new to science. Shape analysis and traditional morphometrics showed concordant patterns with the genetic lineages, with divergent trajectories of skull shape development amongst genetic lineages. The complex contemporary pattern of sympatric distributions amongst Indo-Australasian Miniopterus is the result of the early divergence of the lineage into size-related genetic lineages and subsequent radiation that involved secondary contacts after completion of reproductive isolation. Amongst the many taxa there is evidence for allopatric speciation, incipient groups, one possible example of sympatric speciation on Java (a nexus point in this history of diversification where seven species now exist, with five in syntopy), and ecological speciation—suggesting a mixture of neutral and adaptive processes. While Miniopterus is relatively vagile, and, like Pteropus, has reached the eastern extremes of Australasia (South Australia) and Melanesia (New Caledonia), but unlike Pteropus a prerequisite for subsequent speciation was the crossing of lines of faunal discontinuity during periods of low sea level rather than over-water dispersal to remote land masses. There is still much to know about how sympatric Miniopterus partition themselves ecologically, and therefore whether speciation in at least some cases was the result of adaptive processes. This remarkable radiation will serve as an important comparator for future studies of bat diversification in the region.