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URSID SYSTEMATICS a Brief History of Taxonomy

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URSID SYSTEMATICS a Brief History of Taxonomy HANGINGBEARS FROMPHYLOGENETIC TREES: INVESTIGATINGPATTERNS OF MACROEVOLUTION JOHNL. GITTLEMAN,' Department of Ecologyand EvolutionaryBiology, University of Tennessee, Knoxville,TN 37996, USA Abstract: Phylogeneticinformation of the family Ursidaeis well resolvedand readily available for investigatingmacroevolutionary questions. Using completephylogenies of the ursidsand related terrestrial carnivores, I investigatewhether patterns of body size andlife historyevolution in bearsdiffer fromother carnivores with respectto cladogenesis,species richness,and overall phyletic trends. Largebody size in bearsis not relatedto theirphyloge- netic history,in contrastto most othercarnivore taxa; this may relateto bears' relativelyrecent evolutionary history or theirlarge body size, which is flexible for utilizinglow-quality foods, thusbuffering environmental change. Also, ratesof body size evolutionin bearsare average or perhapsslightly slower thanother carnivores. Certain life historytraits (birth weight, age eyes open, inter-birthinterval, longevity) arevery differentin bearsrelative to other carnivores,even after accountingfor body size and phylogeny. In general,large body size, flexibility in phyletic change in size, and slow life historiesof ursidsmay be an effective evolutionarystrategy for dealingwith recentenvironmental stresses. Ursus 11:29-40 Key words: bears,body size, life history,macroevolution, Ursidae Bears are evolutionarilyrelated to terrestrialcarnivores lytical techniquescan be used to test macroevolutionary including canids, mustelids, hyaenas, and felids. Sys- hypotheses using phylogenies. tematically, ursids are separatedfrom these other taxa Two caveats are needed. Many of the patternsdetected by: (1) unspecialized incisors and molars with broad, here are preliminary;validity will rest with more and flat, tuberculatedcrowns; (2) the shearing function of betterdata. Also, emphasisis placed on patternsof mac- carassials in ancestraltaxa largely replacedby a crush- roevolutionarydifferences between bears and other car- ing function; (3) large and powerful legs, with planti- nivores rather than explanations for these differences. gradeposture; (4) an omnivorousdiet, with most species Futurework, especially at the populationlevel, will sort leaning towardfrugivory and folivory; and, (5) most dis- out why bears are unique. tinctive of all, a gigantic body. Clearly, these features are not only useful for systematics,they also elicit inter- esting ecological and evolutionaryquestions. Does large URSIDSYSTEMATICS body size in bearscontribute to higherextinction (or lower speciation) rates relative to other carnivores? Are bears A BriefHistory of Taxonomy hampered reproductively with respect to life histories Reviews of ursid systematics are found elsewhere becauseof the lengthof time it takesto grow large? These (Simpson 1945; Ewer 1973; Stains 1984; Flynn et al. questions are comparativein nature,specifically requir- 1988; Wayne et al. 1989; Wozencraft 1989a,b; Flynn ing detailed informationabout relative differences with 1996). Excluding the giant (Ailuropodamelanoleuca) other carnivore species and knowledge of evolutionary andred (Ailurusfulgens)pandas, the family Ursidaecom- history. prises the following species: Fortunately,we now have considerable information Helarctos malayanus, Malayan sun bear frombasic naturalhistory field studiesand, more recently, Melursus ursinus, sloth bear fromphylogenetic systematics. Armedwith phylogenetic Tremarctosornatus, Andean (spectacled) bear trees, we can examine the timing and patternof macro- Ursus americanus, Americanblack bear evolutionary changes among bears and closely related Ursus arctos, brown bear lineages. In this paper, I present findings from recent Ursus maritimus,polar bear studies comparingtrends in bears relative to other carni- Ursus thibetanus,Asiatic black bear vores with respect to: (1) phylogenetic trees, (2) macro- Relative to other carnivorefamilies, the taxonomy of evolutionarytrends of speciation and body size changes bears is uncontroversial. Ursidae is one of the most re- using these trees, and (3) variationin life historypaterns. cent taxonomicunits for familial designationin the class My aim is to show how bears differ from other carni- Mammalia (Simpson 1945), the last family of arctoids vores as well as to illustrateby example how mod ana- to appearin the fossil record (Stains 1984), and one of 1 Presentaddress: Department of Biology, GilmerHall, Universityof Virginia,Charlottesville, VA 22903-2477, USA, e-mail: JLGittleman@ Virginia.edu 30 Ursus 11:1999 the most homogeneous Carnivoranfamilies, as reflected Table 1. Indices relating to the distribution of taxonomic minimal subfamilial levels coverage for and the resolution of a composite tree of the by (i.e., Tremarctinae) (see Carnivora Bininda-Emonds et al. The in (from 1999). Wozencraft1989b, 1993). Populationvariance many parenthetical value of percent resolution for the herpestids ursids is significant and continues to be assessed, par- refers to when safe taxonomic reduction(Wilkinson 1995) was ticularly in the brown bear and polar bear (see Wayne used to improve the resolution of this family and Kurten and Anderson Koepfli 1996). Indeed, Number (1980:184) exclaimed in referenceto brown and grizzly of Numberof Percent Elements/ sourcetree/ source elements resolution taxon taxon bear systematics: "Some 232 Recent and 39 fossil "spe- Taxon trees cies" and "subspecies"(list in Erdbrink,1953) have been Higher groups 62 202 100 16.8 0.27 for this taxon-a waste of effortwhich, proposed systematic Mustelidae 30 155 72.7 3.4 0.11 as far as we is with the know, unparalled.".Fortunately, Otariidae 15 46 69.2 3.3 0.22 of some names above list- exception generic (see species Phocidae 21 118 94.4 6.2 0.30 and identification ing; also, Zhang Ryder 1993), species Ursidae 28 50 85.7 6.2 0.22 is the is not stable;therefore, present analysis hampered Canidae 36 180 69.7 5.3 0.15 Of course, there is debate about by species uncertainty. Felidae 40 282 97.1 7.8 0.20 taxonomic placementof the pandas,especially the giant Hyaenidae 6 8 66.7 2.0 0.33 panda,which sharesmany features(herbivorous, planti- Herpestidae 9 53 27.8 1.4 0.16 grade and gigantic) with ursids (O'Brien et al. 1985, (58.3) 1991; Schaller et al. 1985; Mayr 1986.) Both familial Viverridae 9 90 97 2.6 0.29 and ordinalanalyses (e.g., Wyss and Flynn 1993, Zhang and Ryder 1993, Vranaet al. 1994, Bininda-Emondset gruence among phylogenies places the giant panda and al. 1999) stronglyindicate that the giant pandais closely Andean (spectacled)bear as initial lineages in ursidevo- relatedto the bears. The red pandais more of an enigma, lution, the sloth bear as an ancient monotypic lineage, as it arguably can be placed in its own family, in the and the black and polar bears as recent taxa. Also, Procyonidae or in the Ursidae (Roberts and Gittleman throughoutthe family,there is completeresolution among 1984, Bininda-Emondset al. 1999). The comparative nodes, a major improvementfrom one of the first mo- analyses presentedhere will consider the red pandaas a lecular phylogenies (see Wayne et al. 1989). Of course, procyonidbecause of the manyfunctional characters sug- with the many phylogenies available for the ursids and gesting this placementand to not obscureobserved trends no clear methods for how to weight some characters(or between the ursids and other carnivores. phylogenies) against others, it is important to assess agreementamong all the availablephylogenetic hypoth- Phylogenies:Molecular and eses. Morphological Due to the relatively small numberof taxa, accessibil- A CompletePhylogeny Bininda-Emondset al. assembled a ity of sample material,the extendedtime thatbears have (1999) complete for all 271 of derivedfrom evolved, and a fairly complete fossil record,ursids have phylogeny species Carnivora, 166 matrix with received a greatdeal of phylogeneticstudy (Martin1989, phylogenies using representation parsi- Wayne et al. 1989). At least 28 phylogenetic trees are mony analysis (Baum 1992, Ragan 1992). Essentially, combination of available for ursids (Table 1), which is a relatively high matrix representationpermits phyloge- netic treesderived from various data sources, even numbercompared to other carnivorefamilies, consider- though the data not be different and ing the numberof species. Further,many differenttypes may congruent; phylogenies are of characters,including morphological, molecular, and elements given equal weighting. source trees are available for carnivore behavioral and ecological elements, have been used in Most "higher" ursids have the fourth numberat the fam- phylogenetic studies (Wayne et al. 1989, Wozencraft taxa; greatest and mustelids 1989a, Bininda-Emondset al. 1999). As for all organ- ily level behind felids, canids, (Table 1). The that have been studiedmost also isms (Page and Holmes 1998), molecular phylogenies groups intensively tend to have the most elements used for recently have become plentiful for ursids; for example, study, although the ursids behind in this A expla- new phylogenies for the entire family are availablefrom lag respect. possible nation for this trend is that material is less cytochromeb gene (Zhang and Ryder 1993), combined postcranial accessible for such animals as bears, due to cytochrome b/tRNAPro and tRNAThrgenes (Talbot and large-bodied difficulties in and them in mu- Shields 1996), and partial sequence informationfrom 6 the transporting housing seum collections. Ursids however, favor- regions of mtDNA
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