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

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.

[1]  A. Yoder,et al.  Ecology and morphology of mouse lemurs (Microcebus spp.) in a hotspot of microendemism in northeastern Madagascar, with the description of a new species , 2020, American journal of primatology.

[2]  W. Funk,et al.  Coalescent-based species delimitation is sensitive to geographic sampling and isolation by distance , 2020 .

[3]  K. Winker,et al.  An empirical examination of sample size effects on population demographic estimates in birds using single nucleotide polymorphism (SNP) data , 2020, bioRxiv.

[4]  U. Radespiel,et al.  Identification of crucial stepping stone habitats for biodiversity conservation in northeastern Madagascar using remote sensing and comparative predictive modeling , 2020, Biodiversity and Conservation.

[5]  W. Jetz,et al.  Inferring the mammal tree: Species-level sets of phylogenies for questions in ecology, evolution, and conservation , 2019, PLoS biology.

[6]  L. Chikhi,et al.  Genetic and morphological diversity of mouse lemurs (Microcebus spp.) in northern Madagascar: The discovery of a putative new species? , 2019, American journal of primatology.

[7]  G. Besnard,et al.  Late Miocene origin and recent population collapse of the Malagasy savanna olive tree (Noronhia lowryi) , 2019, Biological Journal of the Linnean Society.

[8]  A. Yoder,et al.  Comparative Genomic Analysis of the Pheromone Receptor Class 1 Family (V1R) Reveals Extreme Complexity in Mouse Lemurs (Genus, Microcebus) and a Chromosomal Hotspot across Mammals , 2019, Genome biology and evolution.

[9]  E. Zimmermann,et al.  An empirical estimate of the generation time of mouse lemurs , 2019, American journal of primatology.

[10]  R. Vilà,et al.  The conundrum of species delimitation: a genomic perspective on a mitogenetically super-variable butterfly , 2019, Proceedings of the Royal Society B.

[11]  Austin H. Patton,et al.  Contemporary Demographic Reconstruction Methods Are Robust to Genome Assembly Quality: A Case Study in Tasmanian Devils , 2019, Molecular biology and evolution.

[12]  J. Thorne,et al.  Pedigree-based measurement of the de novo mutation rate in the gray mouse lemur reveals a high mutation rate, few mutations in CpG sites, and a weak sex bias , 2019, bioRxiv.

[13]  I. Kitching,et al.  Genome-wide SNP Data Reveal an Overestimation of Species Diversity in a Group of Hawkmoths , 2019, Genome biology and evolution.

[14]  H. Ellegren,et al.  Genotype‐free estimation of allele frequencies reduces bias and improves demographic inference from RADSeq data , 2019, Molecular ecology resources.

[15]  R. J. Rundell,et al.  The Ecology of Nonecological Speciation and Nonadaptive Radiations. , 2019, Trends in ecology & evolution.

[16]  Jared O'Connell,et al.  Tracking human population structure through time from whole genome sequences , 2019, bioRxiv.

[17]  Melanie Merritt,et al.  What Are Biodiversity Hotspots? , 2019, Front. Young Minds..

[18]  J. McCormack,et al.  Dense geographic and genomic sampling reveals paraphyly and a cryptic lineage in a classic sibling species complex , 2018, bioRxiv.

[19]  O. Mazet,et al.  The IICR and the non-stationary structured coalescent: towards demographic inference with arbitrary changes in population structure , 2018, Heredity.

[20]  S. Willis,et al.  These aren’t the loci you’e looking for: Principles of effective SNP filtering for molecular ecologists , 2018, Molecular ecology.

[21]  Xiyun Jiao,et al.  Species Tree Inference with BPP Using Genomic Sequences and the Multispecies Coalescent , 2018, Molecular biology and evolution.

[22]  E. Zimmermann,et al.  Variation in reproduction of the smallest‐bodied primate radiation, the mouse lemurs (Microcebus spp.): A synopsis , 2018, American journal of primatology.

[23]  P. Unmack,et al.  dartr: An r package to facilitate analysis of SNP data generated from reduced representation genome sequencing , 2018, Molecular ecology resources.

[24]  H. Lumbsch,et al.  Testing the impact of effective population size on speciation rates – a negative correlation or lack thereof in lichenized fungi , 2018, Scientific Reports.

[25]  G. Besnard,et al.  Grass diversification in Madagascar: In situ radiation of two large C3 shade clades and support for a Miocene to Pliocene origin of C4 grassy biomes , 2018 .

[26]  Jeremy M. Brown,et al.  Impact of Model Violations on the Inference of Species Boundaries Under the Multispecies Coalescent , 2018, Systematic biology.

[27]  Tat-Jun Chin,et al.  A comprehensive genomic history of extinct and living elephants , 2018, Proceedings of the National Academy of Sciences.

[28]  S. Ho,et al.  Comparison of Methods for Molecular Species Delimitation Across a Range of Speciation Scenarios , 2018, Systematic biology.

[29]  Tianqi Zhu,et al.  The Spectre of Too Many Species , 2018, bioRxiv.

[30]  W. Salzburger,et al.  Bayesian Divergence-Time Estimation with Genome-Wide Single-Nucleotide Polymorphism Data of Sea Catfishes (Ariidae) Supports Miocene Closure of the Panamanian Isthmus , 2018, Systematic biology.

[31]  P. Etter,et al.  A southern African origin and cryptic structure in the highly mobile plains zebra , 2018, Nature Ecology & Evolution.

[32]  Neva C. Durand,et al.  Hybrid de novo genome assembly and centromere characterization of the gray mouse lemur (Microcebus murinus) , 2017, BMC Biology.

[33]  O. Mazet,et al.  The IICR (inverse instantaneous coalescence rate) as a summary of genomic diversity: insights into demographic inference and model choice , 2017, Heredity.

[34]  L. Chikhi,et al.  Mouse lemurs’ and degraded habitat , 2017, bioRxiv.

[35]  O. Mazet,et al.  The IICR (inverse instantaneous coalescence rate) as a summary of genomic diversity: insights into demographic inference and model choice , 2017, Heredity.

[36]  Ziheng Yang,et al.  Using Phylogenomic Data to Explore the Effects of Relaxed Clocks and Calibration Strategies on Divergence Time Estimation: Primates as a Test Case , 2017, bioRxiv.

[37]  Luay Nakhleh,et al.  Co-estimating Reticulate Phylogenies and Gene Trees from Multi-locus Sequence Data , 2017, bioRxiv.

[38]  L. Chikhi,et al.  Climate change and human colonization triggered habitat loss and fragmentation in Madagascar , 2017, Molecular Ecology.

[39]  Jeet Sukumaran,et al.  Multispecies coalescent delimits structure, not species , 2017, Proceedings of the National Academy of Sciences.

[40]  Niklaus J Grünwald,et al.  vcfr: a package to manipulate and visualize variant call format data in R , 2017, Molecular ecology resources.

[41]  Luis D. Verde Arregoitia,et al.  Impending extinction crisis of the world’s primates: Why primates matter , 2017, Science Advances.

[42]  Brian C. O'Meara,et al.  Species Delimitation with Gene Flow , 2016, Systematic biology.

[43]  Tianqi Zhu,et al.  Maximum Likelihood Implementation of an Isolation‐with‐Migration Model for Three Species , 2016, Systematic biology.

[44]  A. Yoder,et al.  Geogenetic patterns in mouse lemurs (genus Microcebus) reveal the ghosts of Madagascar's forests past , 2016, Proceedings of the National Academy of Sciences.

[45]  F. Forest,et al.  Madagascar's grasses and grasslands: anthropogenic or natural? , 2016, Proceedings of the Royal Society B: Biological Sciences.

[46]  James Mallet,et al.  How reticulated are species? , 2015, BioEssays : news and reviews in molecular, cellular and developmental biology.

[47]  O. Mazet,et al.  On the importance of being structured: instantaneous coalescence rates and human evolution—lessons for ancestral population size inference? , 2015, Heredity.

[48]  G. Luikart,et al.  RAD Capture (Rapture): Flexible and Efficient Sequence-Based Genotyping , 2015, Genetics.

[49]  Mario dos Reis,et al.  The impact of ancestral population size and incomplete lineage sorting on Bayesian estimation of species divergence times , 2015 .

[50]  Evgeny M. Zdobnov,et al.  BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs , 2015, Bioinform..

[51]  S. Gonen,et al.  Exploring the utility of cross-laboratory RAD-sequencing datasets for phylogenetic analysis , 2015, BMC Research Notes.

[52]  L. Godfrey,et al.  Unpredictable environments, opportunistic responses: Reproduction and population turnover in two wild mouse lemur species (Microcebus rufus and M. griseorufus) from eastern and western Madagascar , 2015, American journal of primatology.

[53]  Jason L. Brown,et al.  Shifting ranges and conservation challenges for lemurs in the face of climate change , 2015, Ecology and evolution.

[54]  J. Tobias,et al.  Dispersal and the transition to sympatry in vertebrates , 2015, Proceedings of the Royal Society B: Biological Sciences.

[55]  L. Kubatko,et al.  Quartet Inference from SNP Data Under the Coalescent Model , 2014, Bioinform..

[56]  R. Nielsen,et al.  ANGSD: Analysis of Next Generation Sequencing Data , 2014, BMC Bioinformatics.

[57]  Brian D. Gerber,et al.  Teeth, Sex, and Testosterone: Aging in the World's Smallest Primate , 2014, PloS one.

[58]  C. Hsieh,et al.  Influence of gene flow on divergence dating – implications for the speciation history of Takydromus grass lizards , 2014, Molecular ecology.

[59]  L. Dávalos,et al.  Sex-biased dispersal produces high error rates in mitochondrial distance-based and tree-based species delimitation , 2014 .

[60]  R. Durbin,et al.  Inferring human population size and separation history from multiple genome sequences , 2014, Nature Genetics.

[61]  Matteo Fumagalli,et al.  ngsTools: methods for population genetics analyses from next-generation sequencing data , 2014, Bioinform..

[62]  T. Reeder,et al.  Species delimitation using Bayes factors: simulations and application to the Sceloporus scalaris species group (Squamata: Phrynosomatidae). , 2014, Systematic biology.

[63]  L. Knowles,et al.  Upstream analyses create problems with DNA-based species delimitation. , 2014, Systematic biology.

[64]  D. Edwards,et al.  Species detection and individual assignment in species delimitation: can integrative data increase efficacy? , 2014, Proceedings of the Royal Society B: Biological Sciences.

[65]  Jeffrey D. Lozier,et al.  Revisiting comparisons of genetic diversity in stable and declining species: assessing genome‐wide polymorphism in North American bumble bees using RAD sequencing , 2014, Molecular ecology.

[66]  Alexandros Stamatakis,et al.  RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies , 2014, Bioinform..

[67]  E. Zimmermann,et al.  Species concepts, diversity, and evolution in primates: Lessons to be learned from mouse lemurs , 2014, Evolutionary anthropology.

[68]  R. Bouckaert,et al.  Species Delimitation using Genome-Wide SNP Data , 2013, bioRxiv.

[69]  D. R. Matute,et al.  The role of founder effects on the evolution of reproductive isolation , 2013, Journal of evolutionary biology.

[70]  Michael Roberts,et al.  The MaSuRCA genome assembler , 2013, Bioinform..

[71]  T. Korneliussen,et al.  Estimating Individual Admixture Proportions from Next Generation Sequencing Data , 2013, Genetics.

[72]  Rasmus Heller,et al.  The Confounding Effect of Population Structure on Bayesian Skyline Plot Inferences of Demographic History , 2013, PloS one.

[73]  Ziheng Yang,et al.  Improved Reversible Jump Algorithms for Bayesian Species Delimitation , 2013, Genetics.

[74]  Swapan Mallick,et al.  Ancient Admixture in Human History , 2012, Genetics.

[75]  Tianqi Zhu,et al.  Maximum likelihood implementation of an isolation-with-migration model with three species for testing speciation with gene flow. , 2012, Molecular biology and evolution.

[76]  Check-in-London Kew Royal Botanical Gardens , 2012 .

[77]  Craig Moritz,et al.  Coalescent-based species delimitation in an integrative taxonomy. , 2012, Trends in ecology & evolution.

[78]  Anders Eriksson,et al.  Effect of ancient population structure on the degree of polymorphism shared between modern human populations and ancient hominins , 2012, Proceedings of the National Academy of Sciences.

[79]  Jun Wang,et al.  SNP Calling, Genotype Calling, and Sample Allele Frequency Estimation from New-Generation Sequencing Data , 2012, PloS one.

[80]  L. Chikhi,et al.  Genetic data suggest a natural prehuman origin of open habitats in northern Madagascar and question the deforestation narrative in this region , 2012, Proceedings of the National Academy of Sciences.

[81]  P. Nosil,et al.  The genomics of speciation-with-gene-flow. , 2012, Trends in genetics : TIG.

[82]  S. Sabine,et al.  Acoustic divergence in the communication of cryptic species of nocturnal primates (.)-2 , 2011 .

[83]  Thibaut Jombart,et al.  adegenet 1.3-1: new tools for the analysis of genome-wide SNP data , 2011, Bioinform..

[84]  A. Siepel,et al.  Bayesian inference of ancient human demography from individual genome sequences , 2011, Nature Genetics.

[85]  M. Brameier,et al.  On species delimitation: Yet another lemur species or just genetic variation? , 2011, BMC Evolutionary Biology.

[86]  M. DePristo,et al.  A framework for variation discovery and genotyping using next-generation DNA sequencing data , 2011, Nature Genetics.

[87]  B. Goossens,et al.  The Confounding Effects of Population Structure, Genetic Diversity and the Sampling Scheme on the Detection and Quantification of Population Size Changes , 2010, Genetics.

[88]  Bryan C. Carstens,et al.  Species Delimitation Using a Combined Coalescent and Information-Theoretic Approach: An Example from North American Myotis Bats , 2010, Systematic biology.

[89]  B. Rannala,et al.  Bayesian species delimitation using multilocus sequence data , 2010, Proceedings of the National Academy of Sciences.

[90]  A. Yoder,et al.  Delimiting Species without Nuclear Monophyly in Madagascar's Mouse Lemurs , 2010, PloS one.

[91]  James M. Maley,et al.  Next-generation sequencing reveals phylogeographic structure and a species tree for recent bird divergences. , 2009, Molecular phylogenetics and evolution.

[92]  David H. Alexander,et al.  Fast model-based estimation of ancestry in unrelated individuals. , 2009, Genome research.

[93]  Cole Trapnell,et al.  Ultrafast and memory-efficient alignment of short DNA sequences to the human genome , 2009, Genome Biology.

[94]  Louise S. Mead,et al.  Drift Promotes Speciation by Sexual Selection , 2009, Evolution; international journal of organic evolution.

[95]  L. Rakotozafy,et al.  Exceptional diversity of mouse lemurs (Microcebus spp.) in the Makira region with the description of one new species , 2008, American journal of primatology.

[96]  K. de Queiroz,et al.  Species concepts and species delimitation. , 2007, Systematic biology.

[97]  A. Yoder,et al.  Multiple nuclear loci reveal patterns of incomplete lineage sorting and complex species history within western mouse lemurs (Microcebus). , 2007, Molecular phylogenetics and evolution.

[98]  E. Zimmermann,et al.  The ever-increasing diversity in mouse lemurs: three new species in north and northwestern Madagascar. , 2007, Molecular phylogenetics and evolution.

[99]  David J. Lohman,et al.  Cryptic species as a window on diversity and conservation. , 2007, Trends in ecology & evolution.

[100]  Kam‐biu Liu,et al.  Late Quaternary paleoenvironmental changes in East Africa: a review of multiproxy evidence from palynology, lake sediments, and associated records , 2006 .

[101]  E. Louis,et al.  Revision of the Mouse Lemurs (Microcebus) of Eastern Madagascar , 2006, International Journal of Primatology.

[102]  S. Goodman,et al.  Biogeographic Evolution of Madagascar's Microendemic Biota , 2006, Science.

[103]  A. Thorne,et al.  Timing and tempo of primate speciation , 2006, Journal of evolutionary biology.

[104]  J. Goudet HIERFSTAT , a package for R to compute and test hierarchical F -statistics , 2005 .

[105]  J. Benstead,et al.  Updated estimates of biotic diversity and endemism for Madagascar , 2005, Oryx.

[106]  M. Beaumont,et al.  Recent developments in genetic data analysis: what can they tell us about human demographic history? , 2004, Heredity.

[107]  S. Goodman,et al.  Biogeography of lemurs in the humid forests of Madagascar: the role of elevational distribution and rivers , 2004 .

[108]  Henry T. Wright,et al.  Environmental change, extinction and human activity: evidence from caves in NW Madagascar , 2003 .

[109]  Ziheng Yang,et al.  Comparison of likelihood and Bayesian methods for estimating divergence times using multiple gene Loci and calibration points, with application to a radiation of cute-looking mouse lemur species. , 2003, Systematic biology.

[110]  Ziheng Yang,et al.  Bayes estimation of species divergence times and ancestral population sizes using DNA sequences from multiple loci. , 2003, Genetics.

[111]  R. Martin,et al.  A molecular approach to comparative phylogeography of extant Malagasy lemurs , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[112]  Y. Attia,et al.  Fossil evidence for an ancient divergence of lorises and galagos , 2003, Nature.

[113]  E. Zimmermann,et al.  Sociogenetic structure in a free-living nocturnal primate population: sex-specific differences in the grey mouse lemur (Microcebus murinus) , 2001, Behavioral Ecology and Sociobiology.

[114]  F. Gasse,et al.  Late Quaternary environmental changes from a pollen and diatom record in the southern tropics (Lake Tritrivakely, Madagascar) , 2001 .

[115]  Jörg U. Ganzhorn,et al.  Taxonomic Revision of Mouse Lemurs (Microcebus) in the Western Portions of Madagascar , 2000, International Journal of Primatology.

[116]  A. Yoder,et al.  Remarkable species diversity in Malagasy mouse lemurs (primates, Microcebus). , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[117]  R. Mittermeier,et al.  Biodiversity hotspots for conservation priorities , 2000, Nature.

[118]  C. Boake,et al.  On the Evolution of Premating Isolation after a Founder Event , 1998, The American Naturalist.

[119]  S. Cepok,et al.  Sympatric Mouse Lemurs in Nort-West Madagascar: A New Rufous Mouse Lemur Species (Microcebus ravelobensis) , 1998, Folia Primatologica.

[120]  W. Maddison Gene Trees in Species Trees , 1997 .

[121]  L. Gould Lemurs of Madagascar , 1996, International Journal of Primatology.

[122]  W. Rice,et al.  LABORATORY EXPERIMENTS ON SPECIATION: WHAT HAVE WE LEARNED IN 40 YEARS? , 1993, Evolution; international journal of organic evolution.

[123]  M. Nei,et al.  Relationships between gene trees and species trees. , 1988, Molecular biology and evolution.

[124]  R. D. Martín,et al.  Adaptive radiation and behaviour of the Malagasy lemurs. , 1972, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[125]  D. Hillis,et al.  The Multispecies Coalescent Over-splits Species in the Case of Geographically Widespread Taxa. , 2019, Systematic biology.

[126]  J. Merilä,et al.  Estimating uncertainty in divergence times among three-spined stickleback clades using the multispecies coalescent. , 2019, Molecular phylogenetics and evolution.

[127]  E. Zimmermann,et al.  Mitogenomics of the family Cheirogaleidae and relationships to taxonomy and biogeography in Madagascar , 2016 .

[128]  E. Zimmermann,et al.  Can behavioral ecology help to understand the divergent geographic range sizes of mouse lemurs , 2016 .

[129]  F. Aujard,et al.  Complete mitochondrial genome of the gray mouse lemur, Microcebus murinus (Primates, Cheirogaleidae). , 2015, Mitochondrial DNA.

[130]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[131]  I. Tattersall Madagascar's Lemurs: Cryptic diversity or taxonomic inflation? , 2007 .

[132]  P. Kappeler,et al.  MORPHOLOGY, BEHAVIOUR AND MOLECULAR EVOLUTION OF GIANT MOUSE LEMURS (MIRZA SPP.) GRAY, 1870, WITH DESCRIPTION OF A NEW SPECIES. , 2005 .

[133]  M. Nei,et al.  Relationships between Gene Trees and Species Trees1 , 1998 .

[134]  J. Moat,et al.  VEGETATION MAPPING AND CLASSIFICATION IN MADAGASCAR (USING GIS): IMPLICATIONS AND RECOMMENDATIONS FOR THE CONSERVATION OF BIODIVERSITY , 1998 .

[135]  A. Raftery,et al.  Bayes factors , 1995 .

[136]  G. B̊ardsen,et al.  The Importance of Being Structured , 1993 .

[137]  Walter Pirovano,et al.  BIOINFORMATICS APPLICATIONS , 2022 .

[138]  K. Anstey,et al.  Cc-by-nc-nd 4.0 International License , 2022 .