Cryptic Patterns of Speciation in Cryptic Primates: Microendemic Mouse Lemurs and the Multispecies Coalescent

Abstract

<jats:title>Abstract</jats:title> <jats:p>Mouse lemurs (Microcebus) are a radiation of morphologically cryptic primates distributed throughout Madagascar for which the number of recognized species has exploded in the past two decades. This taxonomic revision has prompted understandable concern that there has been substantial oversplitting in the mouse lemur clade. Here, we investigate mouse lemur diversity in a region in northeastern Madagascar with high levels of microendemism and predicted habitat loss. We analyzed RADseq data with multispecies coalescent (MSC) species delimitation methods for two pairs of sister lineages that include three named species and an undescribed lineage previously identified to have divergent mtDNA. Marked differences in effective population sizes, levels of gene flow, patterns of isolation-by-distance, and species delimitation results were found among the two pairs of lineages. Whereas all tests support the recognition of the presently undescribed lineage as a separate species, the species-level distinction of two previously described species, M. mittermeieri and M. lehilahytsara is not supported – a result that is particularly striking when using the genealogical discordance index (gdi). Non-sister lineages occur sympatrically in two of the localities sampled for this study, despite an estimated divergence time of less than 1 Ma. This suggests rapid evolution of reproductive isolation in the focal lineages, and in the mouse lemur clade generally. The divergence time estimates reported here are based on the MSC calibrated with pedigree-based mutation rates and are considerably more recent than previously published fossil-calibrated relaxed-clock estimates. We discuss the possible explanations for this discrepancy, noting that there are theoretical justifications for preferring the MSC estimates in this case.</jats:p>

Past environmental changes affected lemur population dynamics prior to human impact in Madagascar

“…S15), and a mutation rate of 1.2 × 10 −811,82,83 . This mutation rate is the most accurate estimate available for mouse lemurs and was calculated from average pedigree-based estimates of seven primate species, including that of one mouse lemur species 83,84 . To evaluate the impact of the relatively low genome-wide coverage in our PSMC inferences, we also ran simulations for variant coverage divergence based on minimum read depth option per site (-d) between 1 and 9 for both study sites.…”

How ancient forest fragmentation and riparian connectivity generate high levels of genetic diversity in a microendemic Malagasy tree

“…Finally, the nuclear genomic diversity is ~20-40 times higher than that estimated in poplar populations across all Eurasia (Ma et al ., 2018). For the sake of an approach-based comparison, the diversity is also twice as large as in five eastern-Madagascar mouse lemurs and two orders of magnitude higher than in African plains zebra both estimated using RADseq data and a GL-based analytical procedure (Pedersen et al ., 2018; Poelstra et al ., 2021). This high genetic diversity is particularly unexpected for a narrowly distributed micro-endemic, and thus threatened, species.…”

Next-generation technologies applied to age-old challenges in Madagascar

“…As "cryptic" species, mouse lemurs (Microcebus) have undergone one of the most dramatic taxonomic expansions within the lemuriform primates, and the number of recognized species has increased from a few to 24 in the last decades (Hotaling et al 2016). Though there has been tentative evidence of species hybridization occurring in sympatry (Hapke et al 2011), there are additional sites where two or more species occur while maintaining lineage specificity (e.g., Poelstra et al 2020;Rakotondranary and Ganzhorn 2011). For species diagnostics, researchers have relied primarily on a handful of mitochondrial marker genes, most notably, cytochrome-b (cytb) (Yoder et al 2016).…”