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doi: 10.1186/1741-7007-6-10.

Multigene phylogeny of the Mustelidae: resolving relationships, tempo and biogeographic history of a mammalian adaptive radiation

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Multigene phylogeny of the Mustelidae: resolving relationships, tempo and biogeographic history of a mammalian adaptive radiation

Klaus-Peter Koepfli et al. BMC Biol..

Abstract

Background: Adaptive radiation, the evolution of ecological and phenotypic diversity from a common ancestor, is a central concept in evolutionary biology and characterizes the evolutionary histories of many groups of organisms. One such group is the Mustelidae, the most species-rich family within the mammalian order Carnivora, encompassing 59 species classified into 22 genera. Extant mustelids display extensive ecomorphological diversity, with different lineages having evolved into an array of adaptive zones, from fossorial badgers to semi-aquatic otters. Mustelids are also widely distributed, with multiple genera found on different continents. As with other groups that have undergone adaptive radiation, resolving the phylogenetic history of mustelids presents a number of challenges because ecomorphological convergence may potentially confound morphologically based phylogenetic inferences, and because adaptive radiations often include one or more periods of rapid cladogenesis that require a large amount of data to resolve.

Results: We constructed a nearly complete generic-level phylogeny of the Mustelidae using a data matrix comprising 22 gene segments (approximately 12,000 base pairs) analyzed with maximum parsimony, maximum likelihood and Bayesian inference methods. We show that mustelids are consistently resolved with high nodal support into four major clades and three monotypic lineages. Using Bayesian dating techniques, we provide evidence that mustelids underwent two bursts of diversification that coincide with major paleoenvironmental and biotic changes that occurred during the Neogene and correspond with similar bursts of cladogenesis in other vertebrate groups. Biogeographical analyses indicate that most of the extant diversity of mustelids originated in Eurasia and mustelids have colonized Africa, North America and South America on multiple occasions.

Conclusion: Combined with information from the fossil record, our phylogenetic and dating analyses suggest that mustelid diversification may have been spurred by a combination of faunal turnover events and diversification at lower trophic levels, ultimately caused by climatically driven environmental changes. Our biogeographic analyses show Eurasia as the center of origin of mustelid diversity and that mustelids in Africa, North America and South America have been assembled over time largely via dispersal, which has important implications for understanding the ecology of mustelid communities.

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Figures

Figure 1
Figure 1
Bayesian consensus phylogram of 14,002 trees (burn-in of 6,000 trees) for the Mustelidae using the GTR + I + G model of DNA substitution. Nodes are numbered (1–41), with bootstrap (ML and MP) and posterior probabilities (BI) in Table 1. Brackets at right show subfamily classification as proposed by Wozencraft [7] (inside) and Fulton and Strobeck [11] and Sato et al [15] (outside). Branch lengths are proportional to number of substitutions per site (scale bar).
Figure 2
Figure 2
Chronogram of the Mustelidae based on Bayesian analysis. Posterior values of branch lengths and divergence times (in millions of years) were estimated using 28.5 MYA as the root age prior and 24 MYA as the minimum age for the crown group, the GTR + I + G model of DNA substitution and the uncorrelated lognormal relaxed molecular clock model (rate of each branch is sampled independently from a lognormal distribution, with rates assumed to be uncorrelated among branches). Nodes are numbered as in Figure 1 and posterior estimates of mean and 95% HPD of divergence times are presented in Table 2. Bars represent 95% HPD around mean estimates of divergence times. Vertical green bars indicate two bursts of diversification. Geological time scale is shown at bottom.
Figure 3
Figure 3
ML phylogeny of Mustelidae showing reconstruction of ancestral areas based on the two-state analysis. Pie charts at nodes show proportional likelihoods that the common ancestor was distributed in the Old World (blue) or New World (red). Proportional likelihood values and associated significance levels for ancestral area reconstructions are presented in Additional file 3. Taxa are colored according to their coding states (see legend). * = occurs in both Old and New World.
Figure 4
Figure 4
ML phylogeny of Mustelidae showing reconstruction of ancestral areas based on the four-state analysis. Pie charts at nodes show proportional likelihoods that the common ancestor was distributed in Africa (purple), Eurasia (red), North America (blue) or South America (green). Proportional likelihood values and associated significance levels for ancestral area reconstructions are presented in Additional file 3. Taxa are colored according to their coding states (see legend). * = occurs in Eurasia and North America; + = occurs in North America and South America; # = occurs in Africa and Eurasia.
Figure 5
Figure 5
Frequency histograms showing distribution of node ages within mustelids and four other vertebrate taxa. Mean node ages for mustelids are based on 28.5 MYA root age and 24 MYA crown age priors (see Table 2). The top panel shows ocean temperature curve (smoothed mean in red) based on global deep-sea oxygen isotope (δO18) records (modified from [60]). The development of full-scale ice-sheets in each hemisphere as well as key changes in vegetation in the northern hemisphere during the Neogene are also shown. Following the Mid-Miocene climatic optimum, forested habitats (A) gave way to more open vegetation habitats such as woodlands and grasslands (B). Taiga forests greatly expand during the Pliocene (C). See the text for further details. PLE. denotes Pleistocene.
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References

    1. Scott WB. A History of Land Mammals in the Western Hemisphere. New York: Macmillan; 1937.
    1. Schluter D. The Ecology of Adaptive Radiation. Oxford: Oxford University Press; 2000.
    1. Givnish TJ, Sytsma KJ. Molecular Evolution and Adaptive Radiation. Cambridge: Cambridge University Press; 1997.
    1. Pocock RI. On the external characters and classification of the Mustelidae. Proc Zool Soc Lond. 1921;1921:803–837.
    1. Simpson GG. The principles of classification and a classification of mammals. Bull Am Mus Nat Hist. 1945;85:1–350.

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