Ancient DNA from giant extinct lemurs confirms single origin of Malagasy primates

Abstract

The living Malagasy lemurs constitute a spectacular radiation of >50 species that are believed to have evolved from a common ancestor that colonized Madagascar in the early Tertiary period. Yet, at least 15 additional Malagasy primate species, some of which were relative giants, succumbed to extinction within the past 2,000 years. Their existence in Madagascar is recorded predominantly in its Holocene subfossil record. To rigorously test the hypothesis that all endemic Malagasy primates constitute a monophyletic group and to determine the evolutionary relationships among living and extinct taxa, we have conducted an ancient DNA analysis of subfossil species. A total of nine subfossil individuals from the extinct genera Palaeopropithecus and Megaladapis yielded amplifiable DNA. Phylogenetic analysis of cytochrome b sequences derived from these subfossils corroborates the monophyly of endemic Malagasy primates. Our results support the close relationship of sloth lemurs to living indriids, as has been hypothesized on morphological grounds. In contrast, Megaladapis does not show a sister-group relationship with the living genus Lepilemur. Thus, the classification of the latter in the family Megaladapidae is misleading. By correlating the geographic location of subfossil specimens with relative amplification success, we reconfirm the global trend of increased success rates of ancient DNA recovery from nontropical localities.Madagascar ͉ phylogeny ͉ subfossil ͉ historical biogeography A t least 15% of living primate species are endemic to Madagascar, an island that comprises Ͻ0.4% of Earth's land surface area. These primates are considered to belong to a single clade (1-4) that descends from a single common ancestor that colonized Madagascar from Africa sometime in the early Tertiary period (5-7). They represent a remarkable array of primate life histories and morphologies and, given our knowledge of their phylogenetic unity and biogeographic history, can be considered a definitive example of Darwinian radiation in geographic isolation. Yet, there is also a considerable number of extinct primates from Madagascar, all identified from subfossil remains. More than 16 species (8) from at least seven genera have been recovered, predominantly from Holocene sites throughout Madagascar (9). Although now extinct, the fact that at least some species existed as recently as 500 years ago (10) and all but the genus Babakotia are known to have existed within the past 2,000 years (11) indicates that they were the evolutionary contemporaries of the living lemurs. What is not clear is whether their phylogenetic relationships to the living lemurs challenge our biogeographic hypotheses of Malagasy primate evolution. If we were to discover that any or all of the extinct Malagasy primates fall outside of the lemuriform clade, then we would have to revise our hypothesis of a single primate colonization of Madagascar.The phylogenetic relationships and behavioral ecology of the subfossil lemurs have been studied extensively by using morpholo...

Implications of lemuriform extinctions for the Malagasy flora

“…Because we used fossil-tip dating techniques and not every individual with genetic data had a fully sequenced mitochondrial genome, we constrained the topology to reflect the relationships inferred by Karanth et al (10). To time-calibrate the phylogeny, we used two fossil-based prior age calibrations following the methodology of Kistler et al (11).…”

“…Folivory was inferred to have evolved independently between one and five times, with phylogenetic analyses of ancient DNA demonstrating that Megaladapis, an extinct folivorous lineage, was not a sister to the strictly folivorous Lepilemur clade. Before molecular phylogenetic analyses, the two lineages were considered to form a monophyletic group on the basis of morphology (10). Thus, whereas folivory was initially assumed to have evolved only once in the putative Lepilemur-Megaladapis clade, ancient DNA analysis has revealed that it must have evolved independently at least twice.…”

“…However, recent advances in ancient DNA sequencing have now made it possible to incorporate extinct lineages into phylogenetic analyses (10,11). These advances yield the possibility for a richer understanding of the evolution of lemuriform feeding strategies and their potential relationship to plant dispersal mechanisms.…”

Extinction and ecological retreat in a community of primates

“…15 N) 1 from extant and recently extinct sympatric lemur species. Isotopic niches reflect aspects of habitat and diet, but in condensed form (e.g.…”

“…Lemurs represent a prodigious radiation of primates in Madagascar [1,2]. Yet many are at risk of extinction [2], and at least 17 species have vanished during the past 2000 years [3].…”