Species discovery and validation in a cryptic radiation of endangered primates: coalescent‐based species delimitation in Madagascar's mouse lemurs

Abstract

Implementation of the coalescent model in a Bayesian framework is an emerging strength in genetically based species delimitation studies. By providing an objective measure of species diagnosis, these methods represent a quantitative enhancement to the analysis of multilocus data, and complement more traditional methods based on phenotypic and ecological characteristics. Recognized as two species 20 years ago, mouse lemurs (genus Microcebus) now comprise more than 20 species, largely diagnosed from mtDNA sequence data. With each new species description, enthusiasm has been tempered with scientific scepticism. Here, we present a statistically justified and unbiased Bayesian approach towards mouse lemur species delimitation. We perform validation tests using multilocus sequence data and two methodologies: (i) reverse-jump Markov chain Monte Carlo sampling to assess the likelihood of different models defined a priori by a guide tree, and (ii) a Bayes factor delimitation test that compares different species-tree models without a guide tree. We assess the sensitivity of these methods using randomized individual assignments, which has been used in bpp studies, but not with Bayes factor delimitation tests. Our results validate previously diagnosed taxa, as well as new species hypotheses, resulting in support for three new mouse lemur species. As the challenge of multiple researchers using differing criteria to describe diversity is not unique to Microcebus, the methods used here have significant potential for clarifying diversity in other taxonomic groups. We echo previous studies in advocating that multiple lines of evidence, including use of the coalescent model, should be trusted to delimit new species.

Geogenetic patterns in mouse lemurs (genus Microcebus ) reveal the ghosts of Madagascar's forests past

“…Highlands species M. lehilahytsara as its sister lineage, also in agreement with previous studies (41,46).…”

“…Maximum likelihood trees for concatenated cytb and cox2 loci largely agree with previous analyses (41,46). Although the mtDNA analysis sampled only 17 of the 24 currently described mouse lemur species, the fundamental pattern found in previous studies is repeated here: Described species are resolved as reciprocally monophyletic, and the phylogeny shows a basal split between a clade formed by M. murinus plus M. griseorufus and all other species.…”

“…Ongoing work from the past two decades has shown conclusively that although the morphological differences among species of mouse lemur can be subtle, their genetic and ecological differences are consistent with an evolutionary radiation that presently contains 24 described species (25,(34)(35)(36)(37)(38)(39)(40)(41)(42)(43)(44)(45)(46), with the basal diversification occurring as long ago as 9-10 Ma (47,48). Several studies have shown strong support for three deep lineages, one that contains M. murinus plus Microcebus griseorufus, another deeply diverged lineage represented by Microcebus ravelobensis, Microcebus danfossi, and Microcebus bongolavensis, and a third lineage that comprises all other mouse lemur species, including strong support for a distal subclade containing M. berthae, Microcebus rufus, and Microcebus myoxinus (41,43,44,49).…”

Congruent population genetic structure but differing depths of divergence for three alpine stoneflies with similar ecology and geographic distributions

“…The demographic history of Z. glacier was best described by a north-to-south migration model, with minimal (and perhaps nonexistent) contemporary gene flow among sub-ranges (Supporting Information Table S3). As such, multi-locus nuclear data paired with coalescent-based species delimitation methods are needed before robust molecular conclusions can be drawn regarding both species boundaries and population genetic patterns (Grummer, Bryson, & Reeder, 2014;Hotaling et al, 2016;Yang & Rannala, 2010). Symbols include: Φ CT = among sub-range structure, Φ SC = within sub-range structure, Φ ST = population-level structure across the full study extent irrespective of group structure, and π = nucleotide diversity averaged over the entire COI locus.…”

Population genetics of mouse lemur vomeronasal receptors: current versus past selection and demographic inference

“…are a highly diverse genus with currently 24 described species [27] that are mostly confined to rather local or regional geographic ranges that are separated from each other by large rivers. Allopatric speciation has therefore been proposed as predominant mechanism of diversification within this genus [28, 29].…”