Suprafamilial Relationships Among Rodentia and the Phylogenetic Effect of Removing Fast-Evolving Nucleotides in Mitochondrial, Exon and Intron Fragments
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BMC Evolutionary Biology BioMed Central Research article Open Access Suprafamilial relationships among Rodentia and the phylogenetic effect of removing fast-evolving nucleotides in mitochondrial, exon and intron fragments Claudine Montgelard*1,3, Ellen Forty1, Véronique Arnal1,3 and Conrad A Matthee2 Address: 1Institut des Sciences de l'Evolution de Montpellier (UMR 5554), Université de Montpellier II, Place Eugène Bataillon, 34095 Montpellier cedex, France, 2Evolutionary Genomics Group, Department of Botany and Zoology, Stellenbosch University, Private Bag X1, Matieland, Stellenbosch 7602, South Africa and 3Current address : Biogéographie et Ecologie des Vertébrés (EPHE), Centre d'Ecologie Fonctionnelle et Evolutive (UMR 5175), 1919 Route de Mende, 34293 Montpellier cedex 5, France Email: Claudine Montgelard* - [email protected]; Ellen Forty - [email protected]; Véronique Arnal - [email protected]; Conrad A Matthee - [email protected] * Corresponding author Published: 26 November 2008 Received: 24 April 2008 Accepted: 26 November 2008 BMC Evolutionary Biology 2008, 8:321 doi:10.1186/1471-2148-8-321 This article is available from: http://www.biomedcentral.com/1471-2148/8/321 © 2008 Montgelard 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: The number of rodent clades identified above the family level is contentious, and to date, no consensus has been reached on the basal evolutionary relationships among all rodent families. Rodent suprafamilial phylogenetic relationships are investigated in the present study using ~7600 nucleotide characters derived from two mitochondrial genes (Cytochrome b and 12S rRNA), two nuclear exons (IRBP and vWF) and four nuclear introns (MGF, PRKC, SPTBN, THY). Because increasing the number of nucleotides does not necessarily increase phylogenetic signal (especially if the data is saturated), we assess the potential impact of saturation for each dataset by removing the fastest-evolving positions that have been recognized as sources of inconsistencies in phylogenetics. Results: Taxonomic sampling included multiple representatives of all five rodent suborders described. Fast-evolving positions for each dataset were identified individually using a discrete gamma rate category and sites belonging to the most rapidly evolving eighth gamma category were removed. Phylogenetic tree reconstructions were performed on individual and combined datasets using Parsimony, Bayesian, and partitioned Maximum Likelihood criteria. Removal of fast-evolving positions enhanced the phylogenetic signal to noise ratio but the improvement in resolution was not consistent across different data types. The results suggested that elimination of fastest sites only improved the support for nodes moderately affected by homoplasy (the deepest nodes for introns and more recent nodes for exons and mitochondrial genes). Conclusion: The present study based on eight DNA fragments supports a fully resolved higher level rodent phylogeny with moderate to significant nodal support. Two inter-suprafamilial associations emerged. The first comprised a monophyletic assemblage containing the Anomaluromorpha (Anomaluridae + Pedetidae) + Myomorpha (Muridae + Dipodidae) as sister clade to the Castorimorpha (Castoridae + Geomyoidea). The second suprafamilial clustering identified a novel association between the Sciuromorpha (Gliridae + (Sciuridae + Aplodontidae)) and the Hystricomorpha (Ctenodactylidae + Hystricognathi) which together represents the earliest dichotomy among Rodentia. Molecular time estimates using a relaxed Bayesian molecular clock dates the appearance of the five suborders nearly contemporaniously at the KT boundary and this is congruent with suggestions of an early explosion of rodent diversity. Based on these newly proposed phylogenetic relationships, the evolution of the zygomasseteric pattern that has been used for a long time in rodent systematics is evaluated. Page 1 of 16 (page number not for citation purposes) BMC Evolutionary Biology 2008, 8:321 http://www.biomedcentral.com/1471-2148/8/321 Background [4,11,21,25] and this agrees with Winge [26] and Tullberg Since the pioneer work of Brandt [1], a wealth of literature [24]. However, a recent paper by Horner et al. [27] based has been devoted to suprafamilial relationships among on the coding regions of the mitochondrial genome disa- rodents. To date, however, no consensus has been reached grees with these suggestions and places Anomaluridae based on morphological or paleontological evidence. (Pedetidae was not included) as a sister taxon of Hystri- Nearly a century after Brandt [1], Simpson ([2], p. 197) cognathi. referred to the order Rodentia and stated that "their rela- tionships are involved in an intricate web of convergence, Evolutionary associations among these five suborders are divergence, parallelism, and other taxonomic pitfalls." not well resolved [3] and even the monophyly of the order has been questioned in the past based on mtDNA analyses The addition of molecular data contributed significantly [28,29]. The notion of paraphyly of the Rodentia, how- in constructing a species tree for the order Rodentia and ever, was short lived and never supported by morphology the most up to date taxonomic arrangement includes at and more comprehensive genetic studies [13,20,30,31]. least 2277 species distributed among 33 families and five Based on available evidence, Carleton and Musser [3], suborders [3]. Recently Huchon et al. [4] recognized the suggested that Sciuromorpha, Myomorpha and Hystrico- Laotian rock rat (Laonastes aenigmamus) from Laos [5] as morpha are well established while the monophyly and/or an additional family Diatomyidae closely related to the phylogenetic position of Castorimorpha and Anomaluro- Ctenodactylidae. Despite this new addition, the number morpha is less secure. Subsequent retroposed SINEs pro- of initially recognized rodent families by Simpson [2] and vided additional evidence for the monophyly of Wood [6] remained fairly stable (for review see [3]). The Myomorpha, Anomaluromorpha and Hystricomorpha number of rodent clades identified above the familial whereas no SINE has been identified for Castorimorpha level, however, led to numerous inconsistencies and con- or Sciuromorpha. A clade including Myomorpha, Anom- troversies (see [7-9]). In the present study we adopted the aluromorpha and Castorimorpha (the "mouse-related most up to date suprafamilial classification as reviewed by clade" as defined by Huchon et al. [20]) was also con- Carleton and Musser [3] who recognize five suborders firmed by several unique SINE insertions [11,32]. Unfor- (Sciuromorpha, Castorimorpha, Myomorpha, Anoma- tunately, no SINE has been found for any relationships luromorpha and Hystricomorpha). among the three members of the "mouse-related clade" (Myomorpha, Anomaluromorpha and Castorimorpha). Hystricomorpha contains 19 families (78 genera and 291 Finally the phylogenetic relationships among the three species), and includes the previously problematic Cteno- major rodent groups: Sciuromorpha, "mouse-related dactylidae [3] and the newly discovered Diatomyidae [4]. clade" and Hystricomorpha are as yet unresolved. The two latter families were identified as the sister taxon of the 17 traditional families comprising the infraorder The introduction of phylogenomics and whole organism Hystricognathi [4,10]. The monophyly of Hystricomor- genome sequencing (thousands of nucleotides or amino pha is currently supported by morphological, paleonto- acids), coupled to the use of probabilistic methods based logical and molecular data (see review in [10-13]). on models of sequence evolution, implicitly led to the Sciuromorpha includes Gliridae, Aplodontidae and Sciu- belief that inconsistency in tree reconstructions will soon ridae. The latter two families are closely related based on be something of the past. However, it is clear now that hard and soft morphological features [14-17], albumin increasing the number of nucleotides does not always immunology [18] and sequence data (for example see solve incongruence in phylogenetics [33-35]. Even phyl- [13,19-21]). The myomorphous Gliridae is regarded as an ogenomic reconstructions can result in biases, and as a early offshoot of Sciuromorpha and this is supported by consequence, produce well supported incorrect tree topol- middle ear anatomy [14], arterial patterns [22]) and pre- ogies (for example [33]). In addition, gene tree recon- vious molecular investigations (for example [19,21,23]). structions are based on numerous implicit assumptions Castorimorpha also comprises three families, Castoridae, that are seldom tested (for example gene orthology, Heteromyidae and Geomyidae. This association was first reversible time homogeneous substitution process, sta- suggested by Tullberg [24] and, although not well sup- tionarity of base composition through time). Violations ported by morphology, has fairly strong molecular sup- of these assumptions may lead to compositional bias, port (for example see [13,19-21]). The two superfamilies, contrasted patterns of saturation and heterogeneous evo- Dipodoidea and Muroidea (including one and six fami- lutionary rates among genes and lineages. Current phylo- lies, respectively) comprise the