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Development and application of a phylogenomic toolkit: resolving the evolutionary history of Madagascar's lemurs.

ABSTRACT: Lemurs and the other strepsirrhine primates are of great interest to the primate genomics community due to their phylogenetic placement as the sister lineage to all other primates. Previous attempts to resolve the phylogeny of lemurs employed limited mitochondrial or small nuclear data sets, with many relationships poorly supported or entirely unresolved. We used genomic resources to develop 11 novel markers from nine chromosomes, representing approximately 9 kb of nuclear sequence data. In combination with previously published nuclear and mitochondrial loci, this yields a data set of more than 16 kb and adds approximately 275 kb of DNA sequence to current databases. Our phylogenetic analyses confirm hypotheses of lemuriform monophyly and provide robust resolution of the phylogenetic relationships among the five lemuriform families. We verify that the genus Daubentonia is the sister lineage to all other lemurs. The Cheirogaleidae and Lepilemuridae are sister taxa and together form the sister lineage to the Indriidae; this clade is the sister lineage to the Lemuridae. Divergence time estimates indicate that lemurs are an ancient group, with their initial diversification occurring around the Cretaceous-Tertiary boundary. Given the power of this data set to resolve branches in a notoriously problematic area of primate phylogeny, we anticipate that our phylogenomic toolkit will be of value to other studies of primate phylogeny and diversification. Moreover, the methods applied will be broadly applicable to other taxonomic groups where phylogenetic relationships have been notoriously difficult to resolve.

SUBMITTER: Horvath JE

PROVIDER: S-EPMC2259113 | biostudies-literature | 2008 Mar

REPOSITORIES: biostudies-literature

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Development and application of a phylogenomic toolkit: resolving the evolutionary history of Madagascar's lemurs.

Horvath Julie E JE Weisrock David W DW Embry Stephanie L SL Fiorentino Isabella I Balhoff James P JP Kappeler Peter P Wray Gregory A GA Willard Huntington F HF Yoder Anne D AD

Genome research 20080201 3

Lemurs and the other strepsirrhine primates are of great interest to the primate genomics community due to their phylogenetic placement as the sister lineage to all other primates. Previous attempts to resolve the phylogeny of lemurs employed limited mitochondrial or small nuclear data sets, with many relationships poorly supported or entirely unresolved. We used genomic resources to develop 11 novel markers from nine chromosomes, representing approximately 9 kb of nuclear sequence data. In comb ...[more]

PMID: 18245770

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Project description:Ultraconserved elements (UCEs) have been successfully used in phylogenomics for a variety of taxa, but their power in phylogenetic inference has yet to be extensively compared with that of traditional Sanger sequencing data sets. Moreover, UCE data on invertebrates, including insects, are sparse. We compared the phylogenetic informativeness of 959 UCE loci with a multi-locus data set of ten nuclear markers obtained via Sanger sequencing, testing the ability of these two types of data to resolve and date the evolutionary history of the second most species-rich subfamily of ants in the world, the Formicinae.Phylogenetic analyses show that UCEs are superior in resolving ancient and shallow relationships in formicine ants, demonstrated by increased node support and a more resolved phylogeny. Phylogenetic informativeness metrics indicate a twofold improvement relative to the 10-gene data matrix generated from the identical set of taxa. We were able to significantly improve formicine classification based on our comprehensive UCE phylogeny. Our divergence age estimations, using both UCE and Sanger data, indicate that crown-group Formicinae are older (104-117 Ma) than previously suggested. Biogeographic analyses infer that the diversification of the subfamily has occurred on all continents with no particular hub of cladogenesis.We found UCEs to be far superior to the multi-locus data set in estimating formicine relationships. The early history of the clade remains uncertain due to ancient rapid divergence events that are unresolvable even with our genomic-scale data, although this might be largely an effect of several problematic taxa subtended by long branches. Our comparison of divergence ages from both Sanger and UCE data demonstrates the effectiveness of UCEs for dating analyses. This comparative study highlights both the promise and limitations of UCEs for insect phylogenomics, and will prove useful to the growing number of evolutionary biologists considering the transition from Sanger to next-generation sequencing approaches.

Project description: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.

Project description:AimGlobal animal populations are in decline due to destruction and degradation of their natural habitat. Understanding the factors that determine the distribution and density of threatened animal populations is therefore now a crucial component of their study and conservation. The Cheirogaleidae are a diverse family of small-bodied, nocturnal lemurs that are widespread throughout the forests of Madagascar. However, many cheirogaleid lemurs are now highly threatened with extinction and the environmental factors that determine their distribution and population density are still little known. Here, I investigated the environmental drivers of Cheirogaleidae population density at genus level.LocationVarious forest sites across Madagascar.MethodsI investigated how six environmental variables affect Cheirogaleidae population density at the genus level via random-effect meta-analyses. I then used a generalized linear mixed-effects model to identify the primary predictors of Cheirogaleidae population density. Finally, I investigated how the population density of this family of lemurs varies between protected and unprotected areas of Madagascar via a GLM analysis.ResultsMy results indicate that the relationships between the tested environmental factors and population density are genus-specific among the Cheirogaleidae. Rather remarkably, the density of Microcebus appears to have a profoundly positive relationship with anthropogenic disturbance and a negative relationship with forest cover, a finding that is also reflected by larger population densities within unprotected areas in comparison with localities within Madagascar's protected area network.Main conclusionsThe results of this study are highly encouraging for the conservation of the Cheirogaleidae and highlight the remarkable resilience of these lemurs to habitat degradation and anthropogenic activity. However, this study also outlines the dearth of knowledge that we have for many species, and why these data are urgently needed to understand the biogeography and ecology of threatened animal populations and implement successful conservation.

Dataset Information

Development and application of a phylogenomic toolkit: resolving the evolutionary history of Madagascar's lemurs.

Publications

Development and application of a phylogenomic toolkit: resolving the evolutionary history of Madagascar's lemurs.

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