Type I Sts Markers Are More Informative than Cytochrome b in Phylogenetic Reconstruction of the Mustelidae (Mammalia: Carnivora)

Abstract

We compared the utility of five nuclear gene segments amplified with type I sequence-tagged site (STS) primers versus the complete mitochondrial cytochrome b (cyt b) gene in resolving phylogenetic relationships within the Mustelidae, a large and ecomorphologically diverse family of mammalian carnivores. Maximum parsimony and likelihood analyses of separate and combined data sets were used to address questions regarding the levels of homoplasy, incongruence, and information content within and among loci. All loci showed limited resolution in the separate analyses because of either a low amount of informative variation (nuclear genes) or high levels of homoplasy (cyt b). Individually or combined, the nuclear gene sequences had less homoplasy, retained more signal, and were more decisive, even though cyt b contained more potentially informative variation than all the nuclear sequences combined. We obtained a well-resolved and supported phylogeny when the nuclear sequences were combined. Maximum likelihood and Bayesian phylogenetic analyses of the total combined data (nuclear and mitochondrial DNA sequences) were able to better accommodate the high levels of homoplasy in the cyt b data than was an equally weighted maximum parsimony analysis. Furthermore, partition Bremer support analyses of the total combined tree showed that the relative support of the nuclear and mitochondrial genes differed according to whether or not the homoplasy in the cyt b gene was downweighted. Although the cyt b gene contributed phylogenetic signal for most major groupings, the nuclear gene sequences were more effective in reconstructing the deeper nodes of the combined tree in the equally weighted parsimony analysis, as judged by the variable-length bootstrap method. The total combined data supported the monophyly of the Lutrinae (otters), whereas the Melinae (badgers) and Mustelinae (weasels, martens) were both paraphyletic. The American badger, Taxidea taxus (Taxidiinae), was the most basal taxon. Because hundreds of type I STS primer sets spanning the complete genomes of the human and mouse have been published and thus represent many independently segregating loci, the potential utility of these markers for molecular systematics of mammals and other groups is enormous.

New Insights into the Evolution of Intronic Sequences of the β-fibrinogen Gene and Their Application in Reconstructing Mustelid Phylogeny

“…Notably, Mustela was found to consistently group with Lutrinae to the exclusion of Martes (BS>85% and PP>0.95), indicating the paraphyly of Mustelinae. The sister-grouping of Mustela with Mustelinae and Lutrinae recovered here was in accordance with the results of previous studies based on analyses of other mito-chondrial and nuclear gene combinations (Sato et al, 2003(Sato et al, , 2004(Sato et al, , 2006Koepfli and Wayne, 2003;Marmi et al, 2004;Delisle and Strobeck, 2005;Flynn et al, 2005;Fulton and Strobeck, 2006;Yonezawa et al, 2007). The traditional view from fossil evidence (Wolsan, 1999) and from morphological data (Hunt, 1974;Wozencraft, 1989;Wyss and Flynn, 1993;Bryant et al, 1993), as well as from mustelid supertree construction (Bininda-Emonds et al, 1999), in which Lutrinae was closer to Mephitinae, was not supported in this study.…”

“…Three synapomorphic substitutions were found to support this relationship in our FGB7 data set. The alternative hypotheses proposed in previous studies, including a closer affinity of Martes to the Lutrinae/Mustela clade inferred from the analysis of mitochondrial genes (Marmi et al, 2004;Delisle and Strobeck, 2005), nuclear genes (Sato et al, 2006;Fulton and Strobeck, 2006), and combined mitochondrial and nuclear genes (Sato et al, 2003;Yonezawa et al, 2007), and the possible sister status of Melinae and Martes inferred from the NJ analysis of Cyt B (Sato et al, 2003) and combined analyses of the five nuclear sequence data sets (Koepfli and Wayne, 2003), were not recovered by any of the present analysis. Evidence from additional genes is necessary to test the current phylogenetic hypothesis, considering that the ML and pBI inferences from the concatenated data set failed to convincingly retain this relationship (ML BS=53% and PP=0.89).…”

“…Phylogenetic relationships among these subfamilies of living mustelids have been hotly disputed in recent studies and are not yet well established (Bininda-Emonds et al, 1999;Sato et al, 2003Sato et al, , 2004Sato et al, , 2006Koepfli and Wayne, 2003;Marmi et al, 2004;Flynn et al, 2005;Yonezawa et al, 2007). The main problem is that Mustelidae represents a typical example of rapid evolutionary radiation and recent speciation events (Koepfli and Wayne, 1998;Marmi et al, 2004), possibly dating back to Oligocene (Wolsan, 1993(Wolsan, , 19992005).…”

Phylogenetic history of mustelid fauna in Taiwan inferred from mitochondrial genetic loci

“…As a whole, shallower interspecific relationships were well supported, with the opposite true for deeper nodes, a phenomenon consistent with the previous notion that the mitochondrial genetic loci suffer from the multiple-substitution problem in the phylogenetic reconstruction of the older past (e.g., Sato et al 2003;. Nonetheless, the relationships we obtained among the four subfamilies studied (Guloninae, (Helictidinae, (Lutrinae, Mustelinae))) are consistent with the findings of recent molecular phylogenetic studies (Koepfli and Wayne 2003;Sato et al , 2006Sato et al , 2009aFulton and Strobeck 2006;Koepfli et al 2008). Interspecific relationships within the subfamilies Mustelinae and Guloninae mostly agreed with previous reports (e.g., Sato et al 2003Sato et al , 2006Sato et al , 2009aKoepfli et al 2008;Wolsan and Sato 2010), although our data showed unprecedented strong support for the phylogenetic position of Mustela kathiah.…”

A new otter of giant size,Siamogale melilutrasp. nov. (Lutrinae: Mustelidae: Carnivora), from the latest Miocene Shuitangba site in north-eastern Yunnan, south-western China, and a total-evidence phylogeny of lutrines

“…Most recent molecular phylogenies of mustelids also place the lutrines near the terminal end of the mustelid tree, but as the sister clade of the genus Mustela (Koepfli & Wayne 1998;Sato et al 2003Sato et al , 2009J. J. Flynn et al 2005;Koepfli et al 2008a), as the sister clade of Ictonychinae (Dragoo & Honeycutt 1997;Koepfli & Wayne 2003;Wolsan & Sato 2010;Sato et al 2012), or as both (Koepfli et al 2008b). If the molecular relationship is correct, then the dental similarities between badgers and otters must be the result of convergences.…”