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DNA Systematics and Evolution of the Artiodactyl Family Bovidae (Phylogeny/Ntdna Sequences/Rrna Genes/Rapid Cladogenesis) MARC W

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DNA Systematics and Evolution of the Artiodactyl Family Bovidae (Phylogeny/Ntdna Sequences/Rrna Genes/Rapid Cladogenesis) MARC W Proc. Natl. Acad. Sci. USA Vol. 89, pp. 3972-3976, May 1992 Evolution DNA systematics and evolution of the artiodactyl family Bovidae (phylogeny/ntDNA sequences/rRNA genes/rapid cladogenesis) MARC W. ALLARD, MICHAEL M. MIYAMOTO, LIANNA JARECKI, FRED KRAuS, AND MICHELE R. TENNANT Department of Zoology, University of Florida, Gainesville, FL 32611-2009 Communicated by Charles G. Sibley, January 17, 1992 (received for review October 29, 1991) ABSTRACT Nine additional sequences from representa- outgroup representatives of the infraorder Pecora (8, 9). The tives ofdierent tribes ofthefamily Bovidae were combined with time of divergence for the bovid tribes [estimates ranging six published artiodactyl sequences to provide orthologous from 7 to 20 MA (7)] suggests that relationships within the mtDNA for investigation ofbovid phylogeny and evolution. Each family should be resolvable with this gene complex, which species was represented by a homologous 2.7-kilobase-pair evolves at a rate suitable for this analysis (10). Of the 14 stretch ofmtDNA for the complete 12S and 16S rRNA genes and commonly recognized tribes of Bovidae, only 3 (Ovibovini, three adjacent tRNA genes. These data, whencompared toother Peleini, and Rupicaprini) were not available for this sequenc- results, provided evidence for a monophyletic Bovidae and for ing study; their later inclusion will provide tests of the two clades within the family: one including the tribes Bosela- hypotheses developed herein. phini, Bovini, and Tragelaphini and another for an Antilo- pini/Neotragini grouping. AU other intrafamilial relationships MATERIALS AND METHODS were only weakly supported. These sequence comparisons sug- mtDNA sequences were collected from nine tribal represen- gest that most bovid tribes originated early in the Miocene with tatives including Aepyceros melampus (AME), Boselaphus all extant lineages present by -16-17 million years ago. Thus, tragocamelus (BTR), Cephalophus maxwelli (CMA), Dam- bovid tribes provide an example ofrapid cladogenesis, following aliscus dorcas (DDO), Gazella thomsoni (GTH), Kobus the origin of families in the infraorder Pecora. ellipsiprymnus (KEL), Madoqua kirki (MKI), Oryx gazella (OGA), and Tragelaphus imberbis (TIM). mtDNA isolation, The cloning, and subsequent sequencing followed reported pro- family Bovidae (infraorder Pecora, order Artiodactyla) cedures (11). Additionally, large portions of the sequence for includes 128 extant species in 45 recent genera, which are some species were collected by using PCR for amplification further grouped into 14 tribes, with most native to Africa (1). and sequencing of single-stranded DNA (12). Sequences This family includes domesticated forms (goats, sheep, and were compared to those for other bovid and pecoran repre- cattle), the large herding antelopes of the African plains, and sentatives [Bos taurus (BTA) and Capra hircus (CHI) versus the small solitary, territorial forms usually found in more Antilocapra americana (AAM), Cervus unicolor (CUN), forested areas. The family represents the most diverse group Giraffa camelopardalis (GCA), and Hydropotes inermis of large mammals originating since the Miocene and has been (HIN), respectively] (8, 9). The nine additional sequences studied extensively by those interested in paleoecology, bio- were aligned to each other and to the previously reported geography, comparative anatomy, genetics, behavior, and ones, as described before (9, 11). The four representatives physiology (2). Bovids are represented by a rich paleontolog- from the other pecoran families (AAM, CUN, HIN, and ical record; all extant tribes were present by 7 million years ago GCA) were treated as outgroups and were included in the (MA). Yet despite the large amount of information known analyses to root the trees. These four outgroups span the about them, their phylogenetic relationships remain uncertain. taxonomic and mtDNA diversity present in the closest avail- The difficulty has not been in placing extant taxa into able relatives of the bovid study group (3, 9). genera or tribes, but in determining the relationships among Several heuristic approaches implementing the parsimony tribal groups (3). Many attempts have been made to resolve procedure were conducted to find the most-parsimonious the phylogenetic relationships of bovid tribes (Fig. 1), al- (MP) solution, including varying taxon addition, starting though little, if any, consensus has been reached. This tree(s), and branch-swapping procedures. Analyses based on impasse is not simply a disagreement between molecules and all mutations and transversions alone were conducted. Other morphology, because competing morphological (Fig. 1 B, C, approaches tested the stability of the MP results. Subsets of and F) or molecular (Fig. 1 A and D) studies have disagreed the entire 2.7-kilobase-pair stretch (i.e., treating the 12S and among themselves. A convincing phylogenetic hypothesis is 16S rRNA genes alone and for transversions only) were required to maximize the evolutionary importance of the analyzed separately to determine support among the various facts available for bovids. In this study, we present additional analyses. The more conservative changes (i.e., least satu- molecular data in an attempt to provide better resolution of rated) of these subsets are the transversions, which convey intertribal relationships within this family. the most reliable information about the oldest nodes of our The characters for this study are obtained from nucleotide MP sequences for the mitochondrial rRNA gene complex, con- phylogenies (10). Transversions were also used for date sisting of the complete gene sequences for the large 16S and estimates because they have been documented to change small 12S subunits as well as their three flanking tRNAs linearly with time within the Artiodactyla (9). (tRNAPhe, tRNAv", and the 5' end of tRNALCU). Each taxon Bootstrap resampling (based on 1000 resampling events) was therefore represented by -2.7 kilobase pairs of contig- was also conducted to estimate the stability of the MP uous coding mtDNA. In this study, nucleotide sequences* for topologies (13). To determine how many extra steps were nine additional representatives of bovid tribes were added to required to collapse each node, strict consensus trees were the published sequences for 2 other tribes and for four Abbreviations: MA, million years ago; MP, most-parsimonious; MYR, million years. The three-letter abbreviations for the species The publication costs of this article were defrayed in part by page charge are given in Materials and Methods. payment. This article must therefore be hereby marked "advertisement" *The bovid sequences have been deposited in the GenBank data base in accordance with 18 U.S.C. §1734 solely to indicate this fact. (accession nos. M86493-M86501). 3972 Downloaded by guest on September 25, 2021 Evolution: Allard et al. Proc. Natl. Acad. Sci. USA 89 (1992) 3973 A B C index of dispersion [R(t) = (variance)/(mean of the branch Bovini Bovini Bovini lengths for sister lineages)] with values >2.5 taken as evi- Boselaphini -Boselaphini Boselaphini dence of extensive rate heterogeneity (9, 15). For protein Tragelaphini _ Tragelaphini Tragelaphini sequences used in clock calculations, R(t) is usually <2-3. _ Cephalophini Reduncini Mean percent pairwise divergences (+ 2 SE) for transversions Cephalophini - Hippotragini Neotragini alone were graphed for each tribe to the outgroup families to Hippotragini Reduncini Cephalophini test further for rate heterogeneities. These comparisons to Reduncini Antilopini Antilopini the outgroups make the assumption that the four pecoran Antilopini -Neotragini Alcelaphini families represented in this study are equally related to each Neotragini Caprini Aepycerotini other (i.e., the families reflect a star phylogeny or polychot- 4k a Caprini Alcelaphini Hippotragini omy), hypothesis supported by earlier results (9). The oldest fossils ofthe family Bovidae belong to the genus Alcelaphini Aepycerotini Caprini Eotragus, which has been assigned to the tribe Boselaphini Aepycerotini (7). A rate of divergence for this tribe, using transversions E only, was therefore calibrated according to these fossils and Lim Bovini subsequently compared to that calculated from a different set Aepycerotini Boselaphini of artiodactyl sequences (9). Times of divergence within the Tragelaphini Tragelaphini Additional Steps Bovidae were then estimated from these rates, after evalu- Cephalophini Cephalophini Trees All TV ating the extent of rate heterogeneity among the tribes (as Antilopini Antilopini Mutations described above). Neotragini Neotragini A 19 20 B 38 21 RESULTS AND DISCUSSION Caprini Caprini C 45 31 Bovini Alcelaphini D 55 36 Pairwise Comparisons. Percent divergence was calculated E 32 4 for all pairwise comparisons of the 15 artiodactyl represen- Reduncini Aepycerotini tatives. Within the Bovidae, the minimum divergence found Alcelaphini { Hippotragini (8.3%) was for the CMA to KEL comparison; the highest Hippotragini Reduncini (12.1%) was from the comparisons of TIM to DDO and BTR to FIG. 1. Alternative hypotheses for relationships among the Bo- GTH (Table 1, upper diagonal). The most divergent value vidae based on a wide range of morphological and molecular char- for interfamilial comparisons was 13.7% between AAM and acters. (A-E) Previously hypothesized trees. Only those with a DDO, whereas the least divergent pecoran comparison over- majority of tribes represented are included here. (F) Listing of the lapped
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