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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). Nonsister 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.

Global biodiversity is under accelerating threats, and species are succumbing to extinction before being described. Madagascar’s biota represents an extreme example of this scenario, with the added complication that much of its endemic biodiversity is cryptic. Here we illustrate best practices for clarifying cryptic diversification processes by presenting an integrative framework that leverages multiple lines of evidence and taxon-informed cut-offs for species delimitation, while placing special emphasis on identifying patterns of isolation by distance. We systematically apply this framework to an entire taxonomically controversial primate clade, the mouse lemurs (genus Microcebus , family Cheirogaleidae). We demonstrate that species diversity has been overestimated primarily due to the interpretation of geographic variation as speciation, potentially biasing inference of the underlying processes of evolutionary diversification. Following a revised classification, we find that crypsis within the genus is best explained by a model of morphological stasis imposed by stabilizing selection and a neutral process of niche diversification. Finally, by clarifying species limits and defining evolutionarily significant units, we provide new conservation priorities, bridging fundamental and applied objectives in a generalizable framework. A spatial taxonomic framework integrating genomic, morphological, ecological, life history and acoustic data is used to clarify the cryptic evolution of the taxonomically controversial mouse lemur complex, with a view to aiding future conservation of this and other similarly cryptic clades.

Speciation begins when populations become genetically separated through a substantial reduction in gene flow, and it is at this point that a genetically cohesive set of populations attain the sole property of species: the independent evolution of a population-level lineage. The comprehensive delimitation of species within biodiversity hotspots, regardless of their level of divergence, is important for understanding the factors that drive the diversification of biota and for identifying them as targets for conservation. However, delimiting recently diverged species is challenging due to insufficient time for the differential evolution of characters--including morphological differences, reproductive isolation, and gene tree monophyly--that are typically used as evidence for separately evolving lineages. In this study, we assembled multiple lines of evidence from the analysis of mtDNA and nDNA sequence data for the delimitation of a high diversity of cryptically diverged population-level mouse lemur lineages across the island of Madagascar. Our study uses a multi-faceted approach that applies phylogenetic, population genetic, and genealogical analysis for recognizing lineage diversity and presents the most thoroughly sampled species delimitation of mouse lemur ever performed. The resolution of a large number of geographically defined clades in the mtDNA gene tree provides strong initial evidence for recognizing a high diversity of population-level lineages in mouse lemurs. We find additional support for lineage recognition in the striking concordance between mtDNA clades and patterns of nuclear population structure. Lineages identified using these two sources of evidence also exhibit patterns of population divergence according to genealogical exclusivity estimates. Mouse lemur lineage diversity is reflected in both a geographically fine-scaled pattern of population divergence within established and geographically widespread taxa, as well as newly resolved patterns of micro-endemism revealed through expanded field sampling into previously poorly and well-sampled regions.

The factors that limit the distribution of the highly diverse lemur fauna of Madagascar are still debated. We visited an understudied region of eastern Madagascar, a lowland rainforest site (Sahafina, 29–230 m a.s.l.) close to the Mantadia National Park, in order to conduct a survey and collect further distributional data on mouse lemurs. We captured, measured, photographed, and sampled mouse lemurs from the Sahafina forest, performed standard phylogenetic methods based on three mitochondrial DNA genes, and conducted morphometric comparisons in order to clarify their phylogenetic position and taxonomic status. The mouse lemurs from the Sahafina forest could not be assigned to any of the known mouse lemur species and were highly divergent in all molecular analyses from all previously described species. Since they also differed morphometrically from their sister species and from their geographic neighbors, we propose species status and include a species description at the end. This study suggests that M. lehilahytsara may be the first highland specialist among all mouse lemurs. The distribution of the newly described mouse lemur is not fully known, but seems to be rather restricted and highly fragmented, which raises serious conservation concerns.

Because many survivors of mass extinctions do not participate in postrecovery diversifications, and therefore fall into a pattern that can be termed \"Dead Clade Walking\" (DCW), the effects of mass extinctions extend beyond the losses observed during the event itself. Analyses at two taxonomic levels provide a first-order test of the prevalence of DCWs by using simple and very conservative operational criteria. For four of the Big Five mass extinctions of the Phanerozoic, the marine genera that survived the extinction suffered ≈10-20% attrition in the immediately following geologic stage that was significantly greater than the losses sustained in preextinction stages. The stages immediately following the three Paleozoic mass extinctions also account for 17% of all order-level losses in marine invertebrates over that interval, which is, again, significantly greater than that seen for the other stratigraphic stages (no orders are lost immediately after the end-Triassic or end-Cretaceous mass extinctions). DCWs are not evenly distributed among four regional molluscan time-series following the end-Cretaceous extinction, demonstrating the importance of spatial patterns in recovery dynamics. Although biotic interactions have been invoked to explain the differential postextinction success of clades, such hypotheses must be tested against alternatives that include stochastic processes in low-diversity lineages-which is evidently not a general explanation for the ordinal DCW patterns, because postextinction fates are not related to the size of extinction bottlenecks in Paleozoic orders-and ongoing physical environmental changes.

Background Debate continues as to whether allopatric speciation or peripatric speciation through a founder effect is the predominant force driving evolution in vertebrates. The mouse lemurs of Madagascar are a system in which evolution has generated a large number of species over a relatively recent time frame. Here, we examine speciation patterns in a pair of sister species of mouse lemur, Microcebus murinus and M. griseorufus . These two species have ranges that are disparately proportioned in size, with M. murinus showing a much more extensive range that marginally overlaps that of M. griseorufus . Given that these two species are sister taxa, the asymmetric but overlapping geographic ranges are consistent with a model of peripatric speciation. To test this hypothesis, we analyze DNA sequence data from four molecular markers using coalescent methods. If the peripatric speciation model is supported, we predict substantially greater genetic diversity in M. murinus , relative to M. griseorufus . Further, we expect a larger effective population size in M. murinus and in the common ancestor of the two species than in M. griseorufus , with a concomitant decrease in gene tree/species tree incongruence in the latter and weak signs of demographic expansion in M. murinus . Results Our results reject a model of peripatric divergence. Coalescent effective population size estimates were similar for both extant species and larger than that estimated for their most recent common ancestor. Gene tree results show similar levels of incomplete lineage sorting within species with respect to the species tree, and locus-specific estimates of genetic diversity are concordant for both species. Multilocus demographic analyses suggest range expansions for M. murinus , with this species also experiencing more recent population declines over the past 160 thousand years. Conclusions Results suggest that speciation occurred in allopatry from a common ancestor narrowly distributed throughout southwest Madagascar, with subsequent range expansion for M. murinus . Population decline in M. murinus is likely related to patterns of climate change in Madagascar throughout the Pleistocene, potentially exacerbated by continual anthropogenic perturbation. Genome-level data are needed to quantify the role of niche specialization and adaptation in shaping the current ranges of these species.

The species-level diversity of Madagascar’s lemurs has increased hugely over the last two decades, growing from 32 species in 1994 to 102 species in 2014. This growth is primarily due to the application of molecular phylogenetic analyses and the phylogenetic species concept to known populations, and few previously unknown lemur populations have been discovered during this time. We report on a new population of dwarf lemurs ( Cheirogaleus sp.) from Nosy Hara, a 312-ha island in far northern Madagascar, which constitutes the northernmost distribution record for the genus. The dwarf lemurs appeared to show two characteristics of island populations—insular dwarfism and predator naïveté—that suggest a long isolation, and may thus represent an undescribed taxon. If this is the case, the dwarf lemurs of Nosy Hara are probably one of the rarest primate taxa on Earth.

Background Species are viewed as the fundamental unit in most subdisciplines of biology. To conservationists this unit represents the currency for global biodiversity assessments. Even though Madagascar belongs to one of the top eight biodiversity hotspots of the world, the taxonomy of its charismatic lemuriform primates is not stable. Within the last 25 years, the number of described lemur species has more than doubled, with many newly described species identified among the nocturnal and small-bodied cheirogaleids. Here, we characterize the diversity of the dwarf lemurs (genus Cheirogaleus ) and assess the status of the seven described species, based on phylogenetic and population genetic analysis of mtDNA ( cytb + cox2 ) and three nuclear markers ( adora3 , fiba and vWF ). Results This study identified three distinct evolutionary lineages within the genus Cheirogaleus . Population genetic cluster analyses revealed a further layer of population divergence with six distinct genotypic clusters. Conclusion Based on the general metapopulation lineage concept and multiple concordant data sets, we identify three exclusive groups of dwarf lemur populations that correspond to three of the seven named species: C. major , C. medius and C. crossleyi . These three species were found to be genealogically exclusive in both mtDNA and nDNA loci and are morphologically distinguishable. The molecular and morphometric data indicate that C. adipicaudatus and C. ravus are synonymous with C. medius and C. major , respectively. Cheirogaleus sibreei falls into the C. medius mtDNA clade, but in morphological analyses the membership is not clearly resolved. We do not have sufficient data to assess the status of C. minusculus . Although additional patterns of population differentiation are evident, there are no clear subdivisions that would warrant additional specific status. We propose that ecological and more geographic data should be collected to confirm these results.

BACKGROUND: Spatio-temporal distribution patterns of species in response to natural and anthropogenic drivers provide insight into the ecological processes that determine community composition. We investigated determinants of ecological structure in a species assemblage of 4 closely related primate species of the family Cheirogaleidae (Microcebus berthae, Microcebus murinus, Cheirogaleus medius, Mirza coquereli) in western Madagascar by extensive line transect surveys across spatial and temporal heterogeneities with the specific goal of elucidating the mechanisms stabilizing competitive coexistence of the two mouse lemur species (Microcebus spp.). RESULTS: Interspecific competition between the mouse lemurs was indicated by negative spatial associations in degraded habitat and by habitat partitioning along anthropogenic disturbance gradients during dry seasons with resource scarcity. In non-degraded habitat, intraguild predator M. coquereli, but not C. medius, was negatively associated with M. murinus on the population level, whereas its regional distribution overlapped spatially with that of M. berthae. The species’ interspecific distribution pattern across spatial and temporal heterogeneities corresponded to predictions for agent-mediated coexistence and thus confirmed M. coquereli’s stabilizing impact on the coexistence of mouse lemurs. CONCLUSIONS: Interspecific interactions contribute to ecological structure in this cheirogaleid assemblage and determinants vary across spatio-temporal heterogeneities. Coexistence of Microcebus spp. is stabilized by an agent-mediated spatial storage effect: M. coquereli creates refuges from competition for M. berthae in intact habitat, whereas anthropogenic environments provide M. murinus with an escape from resource competition and intraguild predation. Species persistence in the assemblage therefore depends on the conservation of habitat content and context that stabilizing mechanisms rely on. Our large-scale population level approach did not allow for considering all potential functional and stochastic drivers of ecological structure, a key limitation that accounts for the large proportion of unexplained variance in our models.

We report new evidence that bears decisively on a long-standing controversy in primate systematics. DNA sequence data for the complete cytochrome b gene, combined with an expanded morphological data set, confirm the results of a previous study and again indicate that all extant Malagasy lemurs originated from a single common ancestor. These results, as well as those from other genetic studies, call for a revision of primate classifications in which the dwarf and mouse lemurs are placed within the Afro-Asian lorisiforms. The phylogenetic results, in agreement with paleocontinental data, indicate an African origin for the common ancestor of lemurs and lorises (the Strepsirrhini). The molecular data further suggest the surprising conclusion that lemurs began evolving independently by the early Eocene at the latest. This indicates that the Malagasy primate lineage is more ancient than generally thought and places the split between the two strepsirrhine lineages well before the appearance of known Eocene fossil primates. We conclude that primate origins were marked by rapid speciation and diversification sometime before the late Paleocene.