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Taking Measure of Mustelids: Morphological Diversity

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Taking Measure of Mustelids: Morphological Diversity Taking MeasureAuthor's personal copy of Mustelids: 732 I. Agnarsson et al. / Molecular Phylogenetics and Evolution 54 (2010) 726–745 MorphologicalWe use theDiversity Tuatara module (Maddison and Mooers, 2007)in the evolutionary analysis packet Mesquite (Maddison and Maddi- Vormela peregusna Paula Noonan and Virginiason, 2009 Hayssen) to assess conservation, Smith priorities forCollege, carnivoran species. Northampton, MA We illustrate one example of such an analysis in Fig. 8. We calcu- lated (1) evolutionary distinctiveness (ED), a measure of a species The small carnivores of the Mustelidae familyterminal are branchResults length and its share in ancestral branches, morphologically diverse and include weasels,weighted by ‘global extinction’ (GE) risk (=EDGE, Isaac et al., 120 2007) and (2) theData expected reveal terminal that branch while length sexual of species, dimorphism tak- 100 martens, badgers, and otters. Many are ing into accountis thean extinctionoverall probabilitypattern for of all these species, families, again only 80 terrestrial; others are aquatic, fossorial, or weighted by extinction risk (HEDGE, Steel et al., 2007). We calcu- one statistically significant measure is Head body arboreal. Often, they traverse different terrainslate extinction risk by translating IUCN threat categories to extinc- 60 equally well (Gittleman, 1985). Mustelids aretion probabilities,found needed at asthe input family values level: in Tuatara, body using mass the for 40 Tail ‘pessimistic’ approachthe Mustelidae of Mooers et. al. Of (2008) the. Weeight note mustelid that the 20 often thought of as the long, skinny mammals,‘pessimistic’ transformation gives relatively great weight to phylo- from the least weasel (Mustela nivalis) to thegenetic distinctivenesssubfamilies, as all taxa areonly considered the Mustelinae at some consider- (Mustela 0 Hind foot giant otter (Pteronura brasiliensis). However,able risk of extinction.species) To allowshow the significant inclusion of ‘data sexual deficient’ several species stray from this description. species we, arbitrarily, but probably conservatively, estimated their extinctiondimorphism risk as in between across the ‘least five concern’ measures. and ‘near When This family is known for sexual dimorphism.threatened’ categories.sexual As dimorphism emphasized by Mooers is examined et al. (2008) onre- the This study compares the sexual dimorphismsults of of EDGE andspecies HEDGE analyseslevel, arehowever, sensitive to significant how IUCN cat- sexual Mustelidae to its close relatives Potos (the basalegories are translated to extinction probabilities. However, for our purposes of showingdimorphism one potential appears use of this in phylogeny, species we onlyin all three species in a recent phylogeny) and Mephitidae Figure 2. The percent of subspecies of 5 species of illustrate one examplefamilies, of analyzing as well the as data, Potos and note, although that while not and Procyonidae, which are more related to each Mustelidae that show significant sexual dimorphism. results from otheralways types ofconsistently analyses differed across in many details,the morpho the - other than either is to the mustelids (Agnarssontop priority, species for conservation seen in Fig. 8 ranked relatively 2010). high in every analysis.logical measures (Figure 1). At the Discussion subspecies level, the variation continues, Sexual dimorphism can derive from partitioning of resources, 3. Results with some subspecies within a species but also from sexual selection (male-male competition and showing significant sexual dimorphism, 3.1. Benchmark clades female preference) and reproductive efficiency. Any single and others not (Figure 2). factor can influence sexual dimorphism, but the influences The Bayesian analysis of the pruned dataset gave essentially are not mutually exclusive (Hedrick & Temeles, 1989). identical result, differing only in terms of support values, which were typically higher than in the full analysis. Hence, we will con- 100 Although the overall trend of larger males than females fine most of our discussion to the Bayesian analysis including all persists at all taxonomic levels for Mephitidae, Mustelidae, taxa. The phylogeny recovers the monophyly of all benchmark 80 Potos, and Procyonidae, variation in significant sexual clades (Figs. 1, 2 and Table 2). However, the Bayesian result sup- ports a slightly modified60 Arctoidea and Musteloidea, due to theMephitidae dimorphism is not revealed at the family level, but becomes placement of the red panda (Ailurus fulgens, Ailuridae) sister to Fig. 1. Summary of relationships among carnivoran families. Photographs by M. apparent at the subfamily, species, and subspecies levels. Canidae (Fig. 1).40 The likelihood analysis (see Supplementary Kuntner (tiger, hyena,From fossa, Agnarsson panda, wolf, coati, et al., sea lion), 2010. I. Agnarsson (otter, red Fig. 2) recovers the ‘traditional’ Arctoidea, but not Musteloidea,Mustelidae While phylogenetic relatedness may explain the trend toward panda). The following obtained with permission from ASM mammal image library: as it places the red panda sister to a clade containing all Caniformia palm civet (K. Kutunidisz), walrus (J.D. Haweeli), kinkajou (R.D. Lord). The following 20 sexual dimorphism, variations in this pattern may be the photographs areMethods licensed under GFDL, see http://www.gnu.org/copyleft/fdl.html, minus Canidae. In the parsimony analysis the two long branches,Procyonidae genet (Guérin Nicolas), linsang (Alessio Marrucci), meerkat (Fir0002/Flagstaffotos). red panda and kinkajou (Potos flavus) attract. The placement of result of other selective pressures. Photos of elephantData seals (Janfrom Roletto) 7,500 and skunks specimens from public domain.were gathered fromthe red panda has0 not been stable across prior analyses and must be considered unresolved.Head We findTail support Hind for Carnivora,Ear Mass its subdi- museum specimens and the literature. MaximumMeasurements likelihood analyses recorded were conducted were in head-body, the program tail,vision into Caniformiabody and Feliformia,foot and for all but one of the currently recognized families within both suborders. Our Bayesian References Garli (Zwickl,hind 2006), foot, using and the GTR+ earC lengths,+I model and plus 200 body search mass. rep- lications. The best tree (lowest log likelihood) from these 200 anal- and likelihood results are incongruent with current classification at Agnarsson, I., M. Kuntner, and L. J. May-Collado. 2010. Dogs, Trends of sexual dimorphism on the family, the family levelFigure only in 1. the The placement percent of of a singlespecies species, of Mephitidae the , cats, and kin: a molecular species-level phylogeny of Carnivora. yses (see Supplementary Fig. 1) broadly agrees with the Bayesian Mustelidae, and Procyonidae that show results. We focussubfamily, our discussion species, on the and Bayesian subspecies results as levels they werekinkajou which here, instead of nesting within Procyonidae, is sis- Molecular Phylogenetics and Evolution 54: 726-745. simultaneouslyanalyzed provide an in estimate Minitab. of the phylogeny, and support ter to a clade containingsignificant Procyonidae, sexual Mustelidae,dimorphism. and Mephitidae The parsimony results differ further, e.g., placing one cat Gittleman, J. L. 1985. Carnivore body size: ecological and for it. However, we discuss the likelihood results when there are (Fig. 1). (Homotherium serum) with viverrids, Genetta felina (Viverridae, Fel- taxonomic correlates. Oecologia 67(4): 540-554. major differencesAcknowledgments with the Bayesian analysis. iformia) with bears (Ursidae, Caniformia), by uniting the red panda May-Collado and Agnarsson (2006) showed that, in terms of the Hedrick, A. V., and E. J. Temeles. 1989. The evolution of sexual This research was supported by the Horner andFund. kinkajou, The assistance and placing skunks of (Mephitidae) within raccoons recovery of ‘known’ clades (benchmark clades) parsimony per- dimorphism in animals: hypotheses and tests. TREE 4(5): the staffs of the American Museum of Natural(Procyonidae). History, Field These Museum, unlikely relationships in most cases involve formed relatively poorly compared to Bayesian analyses of cytb se- taxa with notably long branches, hence potentially a result of long 136-138. quences withinand Cetartiodactyla. Smithsonian Parsimony collections analyses is gratefully were also acknowledged. branch attraction. Given these issues, we do not discuss the parsi- conducted (see May-Collado and Agnarsson, 2006, for analysis mony analysis further. parameters using parsimony), confirming our previous findings; although overall the results are quite similar, parsimony results are in greater conflict with the available external evidence (mor- 3.2. Caniformia phology, nuclear DNA, mitogenomic studies, etc.) and recover many fewer benchmark clades than Bayesian analyses (see Supple- The Bayesian results suggest a sister relationship between mentary Fig. 1). the red panda (Ailurus fulgens) and Canidae and, in turn, that.
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