Multigene Phylogeny of the Mustelidae: Resolving Relationships
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BMC Biology BioMed Central Research article Open Access Multigene phylogeny of the Mustelidae: Resolving relationships, tempo and biogeographic history of a mammalian adaptive radiation Klaus-Peter Koepfli*1, Kerry A Deere1, Graham J Slater1, Colleen Begg2, Keith Begg2, Lon Grassman3, Mauro Lucherini4, Geraldine Veron5 and Robert K Wayne1 Address: 1Department of Ecology and Evolutionary Biology, University of California, Los Angeles, CA, 90095-1606, USA, 2Postnet Suite 230, Private Bag X18, Rondebosch, 7701, Republic of South Africa, 3Caesar Kleberg Wildlife Research Institute, MSC 218, 700 University Boulevard, Texas A and M University-Kingsville, Kingsville, TX 78363, USA, 4Grupo de Ecología Comportamental de Mammiferos (GECM), Cátedra Fisiología Animal, Departamento de Biología, Bioquímica y Farmacia, Universidad Nacional del Sur – CONICET, San Juan 670, 8000 Bahía Blanca, Argentina and 5Muséum National d'Histoire Naturelle, Département Systématique et Evolution, CP 51 USM 601-UMR 5202, Origine, Structure et Evolution de la Biodiversité, 57 Rue Cuvier, 75231 Paris Cedex 05, France Email: Klaus-Peter Koepfli* - [email protected]; Kerry A Deere - [email protected]; Graham J Slater - [email protected]; Colleen Begg - [email protected]; Keith Begg - [email protected]; Lon Grassman - [email protected]; Mauro Lucherini - [email protected]; Geraldine Veron - [email protected]; Robert K Wayne - [email protected] * Corresponding author Published: 14 February 2008 Received: 29 January 2008 Accepted: 14 February 2008 BMC Biology 2008, 6:10 doi:10.1186/1741-7007-6-10 This article is available from: http://www.biomedcentral.com/1741-7007/6/10 © 2008 Koepfli et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. 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 (~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. Page 1 of 22 (page number not for citation purposes) BMC Biology 2008, 6:10 http://www.biomedcentral.com/1741-7007/6/10 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. Background latter scheme was proposed in recognition of demon- "Wave after wave of immigration came in from Asia, strated paraphyly of the traditional subfamilies by more recruiting the fauna at each successive stage, but leaving recent morphological-based phylogenetic studies [8]. little opportunity for new types to arise here. Even those genera which seem to be of native origin, might prove to During the last decade, DNA sequence-based studies have be immigrants, if all their history were known ([1], p begun to challenge the validity of the five-subfamily 593)." scheme and even monophyly of the family itself. Studies using both mitochondrial and nuclear sequences have The diversification of the Mustelidae (Carnivora, Mam- consistently demonstrated that skunks and stink badgers malia) is a striking example of adaptive radiation, the evo- (Mydaus) descend from a common ancestor and together lution of ecological and phenotypic diversity from a form a lineage (Mephitidae) that diverged prior to the common ancestor [2]. Mustelids exhibit both locomotor split between Mustelidae and Procyonidae [9-11]. These and dietary diversity, with taxa that are fossorial (badg- studies and those more focused on mustelids [12-17] have ers), semi-arboreal (martens) and semi-aquatic (otters), also suggested that: (i) the Lutrinae is monophyletic; but and diets that vary from specialization on rodents (wea- that (ii) both Melinae and Mustelinae are polyphyletic. sels) to piscivory (otters). Ecomorphological diversity in However, phylogenetic relationships within the family the family is thus correspondingly high, reflecting the remain uncertain or unknown because taxon sampling, adaptation of different species of mustelids to different especially for genera, has been incomplete. Further, ade- habits and habitats. As with other cases of adaptive radia- quate character sampling is also an important issue tion [3], resolving relationships within the Mustelidae, because adaptive radiations are often composed of line- especially among genera, has been challenging. Many tax- ages that have rapidly diverged [2,3]. Short stem lengths onomic schemes proposed for mustelids within the last of topologies revealed in recent studies, albeit with century were based on morphology and classified genera incomplete taxon sampling [11,13] suggests that deeper into various numbers of subfamilies [4,5] whose bounda- lineages of mustelids may have radiated within a short ries were largely determined by ecomorphological simi- span of time. Adequate character sampling is therefore larity. At one extreme, Pocock [4] divided extant mustelids critical in achieving an accurate, well-resolved and robust into 15 (mostly monotypic) subfamilies based on descrip- phylogenetic hypothesis. tive analyses of external characters (e.g. structure of the rhinarium and feet). At the other end, the system pro- Fossil evidence indicates that the biogeographic history of posed by Simpson [5] cast mustelids into five subfamilies mustelids is characterized by numerous intercontinental based on both phylogeny and 'similarity in adaptiveness' dispersals, primarily originating from Eurasia where the of constituent genera: Lutrinae (otters), Melinae (badg- earliest fossil remains of the family (of Late Oligocene ers), Mellivorinae (honey badger), Mephitinae (skunks) age) are found [18,19]. For instance, a large majority of and Mustelinae (martens and weasels). While such a mustelid diversity in North (and South) America is con- scheme may indeed reflect the true phylogeny in some sidered to have originated from lineages that repeatedly instances, morphological similarity does not necessarily dispersed from Eurasia via the Bering land bridge [19,20]. imply phylogenetic affinity, as has been well demon- The earliest immigrants to North America arrived in the strated in certain groups that exemplify adaptive radiation Early Miocene and included a paraphyletic group of stem (e.g. Anolis lizards [6]). Moreover, such criteria can lead to taxa referred to as 'paleomustelids', whose affinities to recognition of polyphyletic grades rather than mono- crown group mustelids ('neomustelids') remains ambigu- phyletic groups. Nonetheless, Simpson's subfamilial clas- ous, as well as genera that belonged to the extinct sub- sification of the Mustelidae has been followed for many family Leptarctinae [20-25]. The first appearance of years, although the latest classification provisionally various mustelid genera in North America is used to help places all mustelids (excluding skunks and stink badgers) define the beginning of biostratigraphic boundaries of into two subfamilies, Lutrinae and Mustelinae [7]. This North American land mammal ages (NALMAs) during the Page 2 of 22 (page number not for citation purposes) BMC Biology 2008, 6:10 http://www.biomedcentral.com/1741-7007/6/10 Neogene [19,26]. For example, the first appearance of pelage (Galictis, Ictonyx, Poecilogale and Vormela; node 27).