Department of Zoology, University of Stellenbosch, Stellenbosch, South Africa
Department of Animal Science, Texas A&M University
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Abstract |
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Introduction |
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Following Nowak (1999)
, with slight modifications from the morphological (Gentry 1992
) and current genetic literature (Gatesy et al. 1997
; Hassanin and Douzery 1999a
; Matthee and Robinson 1999
), at least 7 monophyletic subfamilies and more than 12 tribes can be identified. The subfamilies include the earliest-diverging Bovinae (cow, eland, and nilgai group) and the more recent Cephalophinae (duikers), Antilopinae (gazelles, saiga, springbok, steenbok, dik-dik, and oribi group), Caprinae (sheep and goat group), Hippotraginae (roan and gemsbok group), Reduncinae (waterbuck, lechwe, and gray rhebok group), and Alcelaphinae (hartebeest and wildebeest group). Although monophyly of the majority of the subfamilies is supported by morphological data (Vrba 1985
; Kingdon 1989
; Gentry 1992
), fossil evidence (Gentry 1992
), allozymes (Georgiadis, Kat, and Oketch 1990
), serum immunology (Lowenstein 1986
), cytogenetic data (Modi, Gallagher, and Womack 1996
; Robinson et al. 1998
), and DNA sequence analyses (Allard et al. 1992
; Gatesy et al. 1992, 1997
; Geraads 1992
; Groves and Shields 1996
; Janecek et al. 1996
; Essop, Harley, and Baumgarten 1997
; Hassanin and Douzery 1999a, 1999b
; Matthee and Robinson 1999
; Rebholz and Harley 1999
), the evolutionary relationships among most bovid subfamilies remain uncertain.
The systematic description of the group is further clouded by problematic taxa such as the impala (Aepyceros), the suni (Neotragus), and the klipspringer (Oreotragus). In the past, the impala was grouped with the Alcelaphinae (Vrba 1984
; Lowenstein 1986
), with the Antilopinae (Kingdon 1989
), with the Reduncinae (Murray 1984
), or as a distinct subfamily, Aepycerotinae (Ansell 1971
; Vrba 1979
; Gentry 1992
). Although most conventional classification systems place the suni and klipspringer within the dwarf antelope tribe Neotragini (subfamily Antilopinae; see Nowak 1999
), there is no molecular (Hassanin and Douzery 1999a, 1999b
; Matthee and Robinson 1999
) or strong morphological evidence (Oboussier 1979
; Gentry 1992
) to support these findings. A recent cytochrome b study (Matthee and Robinson 1999
) suggested that the klipspringer was a sister taxon to Cephalophinae, a finding initially proposed by Oboussier (1979)
based on brain morphology. Additionally, the molecular cytochrome b data suggested that the suni was a sister taxon to the impala. It is important to realize that statistical support for the above-mentioned associations is weak, and no robust conclusions could thus be reached (Hassanin and Douzery 1999a
; Matthee and Robinson 1999
; Rebholz and Harley 1999
).
Based on cladistic and phenetic analyses of 112 skeletal characters taken from the horn-core, skull, tooth, and postcranium, Gentry (1992)
concluded that bovids cluster around four foci in ascending evolutionary sequence: Bovinae; Antelopinae and some dwarf antelopes; Caprinae; and a group of African antelopes containing the impala, Alcelaphinae, Hippotraginae, and Reduncinae. This conclusion, however, was based on the fact that the early derived bovids (i.e., Bovinae) share more primitive similarities than divergently advanced ones with each other and hence associate more closely. Furthermore, the morphological data demonstrated a low consistency index value clearly indicative of a large degree of parallelism in bovid history (Gentry 1992
).
The incomplete nature of the bovid Miocene fossil record (Vrba 1985
), together with morphological parallelisms (Gentry 1992
) and rapid cladogenesis (Vrba 1985
; Georgiadis, Kat, and Oketch 1990
; Allard et al. 1992
; Gatesy et al. 1997
), led many authors to conclude that the subfamilial relationships within the Bovidae could be resolved only through comprehensive species sampling and by using data derived from multiple sources (Allard et al. 1992
; Gentry 1992
; Gatesy et al. 1997
; Matthee and Robinson 1999
). The retrieval of phylogenetic information from mtDNA data has widely been thought to be confounded by the rapid radiation within the Bovidae (Allard et al. 1992
; Gatesy et al. 1997
; Matthee and Robinson 1999
; Rebholz and Harley 1999
). In the mtDNA molecular analyses, the unresolved nodes persist even when complex weighting schemes are used in an attempt to reduce homoplasy/noise (Gatesy et al. 1997
; Hassanin and Douzery 1999a, 1999b
). Rapid radiations become more problematic as evolutionary time increases (Matthee and Robinson 1997
) and, given the Miocene origin of the Bovidae, might explain why few well-supported associations among bovid subfamilies were retrieved by earlier mtDNA studies.
Nuclear DNA sequence data can offer a powerful alternative to mtDNA data (Robinson et al. 1997
; Stanhope et al. 1998
; Gatesy et al. 1999
; von Dornum and Ruvolo 1999
), and the extension of data from additional sources might provide more robust phylogenies for problematic taxa. The nuclear genome of mammals is approximately 166,000 times as large as the mitochondrial genome and also provides sets of markers that potentially segregate independently. Despite this rich source of data, phylogenetic studies based on nuclear DNA genes remain limited, and the majority of past investigations have been at the higher systematic level (i.e., among orders and families of vertebrates with origins more than 30 MYA; Robinson et al. 1997
; Stanhope et al. 1998
; Gatesy et al. 1999
). A recent artiodactyl investigation by Matthee et al. (2001)
provided a suite of eight nuclear genetic markers that showed potential to resolve systematic uncertainties at both the higher and the lower taxonomic levels in vertebrates (e.g., among subfamilies of vertebrates with origins generally dating back less than 20 Myr). In the present investigation, we were particularly interested in the utility of these nuclear DNA intron sequences in addressing systematic questions at the lower taxonomic level (see above). In this study, we extended our initial investigation of the Artiodactyla by sequencing 4 of the 8 nuclear DNA fragments for an additional 22 bovid taxa.
In an attempt to resolve the phylogeny of the family Bovidae, a complete mitochondrial DNA data set originating from the three mtDNA genes (Gatesy et al. 1997
; Matthee and Robinson 1999
) was also included in combined analyses. The evolutionary rates and selective constraints operating on different DNA genes vary and could therefore potentially have two benefits for this study. First, highly supported nodes retrieved from the analyses of independent and combined nuclear and mitochondrial data can be considered robust (Hillis 1995
). Second, because of different evolutionary rates among nuclear and mtDNA genes, these data should provide phylogenetic signal at different levels of the tree (Halanych and Robinson 1999
; B. Jansen van Vuuren and T. J. Robinson, personal communication). For example, the rapid evolutionary radiations of the Bovidae near the Miocene-Pliocene boundary (the basal and internal radiations of subfamilies; Vrba 1985
) might be better recovered by the nuclear DNA sequences, while phylogenetic signal from the mid-Pleistocene radiations (more terminal nodes/radiation within subfamilies; Vrba 1985
) might be more prominent in the faster-evolving mitochondrial DNA data.
The aims of this investigation were therefore threefold: (1) to investigate the value of conservative nuclear DNA intron sequences in recovering a robust phylogeny for a reasonably closely related group of vertebrates characterized by a rapid radiation, (2) to provide a more robust phylogeny for the bovid subfamilies, and (3) to obtain a nuclear DNA perspective on the puzzling phylogenetic position of the impala, suni, and klipspringer.
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Materials and Methods |
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To obtain comparable taxon sampling between the mtDNA and nuclear DNA data sets, we sequenced an additional 12 mtDNA gene fragments from seven taxa. The universal cytochrome b primers (L14724 and H15915; see Matthee and Robinson 1999
for details) were used to obtain complete gene sequences for the gemsbok (Gazella oryx) and the gerenuk (Litocranius walleri) and the published ribosomal primers (see Gatesy et al. [1997
] for details) were used to generate the missing 12S rRNA and 16S rRNA sequences for the gerenuk (L. walleri), the Cape grysbok (Raphicerus melanotis), Sharp's grysbok (Raphicerus sharpei), the suni (Neotragus moschatus), the gray duiker (Sylvicapra grimmia), and the klipspringer (Oreotragus oreotragus).
PCR procedures followed standard methodology, and the reaction mixes contained approximately 100200 ng total genomic DNA. Variable MgCl2 concentrations (1.02.5 mM) were used to achieve optimal primer annealing and to reduce nonspecific amplification. Before purification with QIAquick (Qiagen Ltd.), a 5-µl sample of each PCR reaction mix was screened on 1% agarose gels, together with a size standard ( cut with HindIII). The purified PCR products were cycle-sequenced using BigDye terminator chemistry (Perkin Elmer, Applied Biosystems), and all of the sequenced products were purified using Centrisep spin columns (Princeton separations) and analyzed on a 377 ABI automated sequencer.
Sequence data were obtained for all genes in all specimens with the exception of the Kap-cas fragment in oribi. Several attempts, including the development of additional primers, failed to amplify the kappa-casein fragment for this taxon. The oribi was therefore excluded from the Kap-cas analyses. The sequence data were verified by sequencing both strands. Heterozygous changes in the nuclear DNA data occurred at low frequencies (less than 0.1% cases) and were confirmed on the chromatograms. They mostly involved transitional changes, and these changes were designated as one of the two possible states based on the frequencies in the other individuals.
Sequence Analyses
All sequences were aligned manually, and the exon/intron boundaries for the nuclear genes were defined using BLASTN searches in GenBank. The aligned database has been deposited in EMBL (accession number DS42701), and all of the individual sequences can be obtained from GenBank (accession numbers AF210154AF210240 and AF249973AF249984). Small areas of ambiguous alignment in the 16S rRNA region (39 characters) were excluded before the phylogenetic analyses were performed. All alignment gaps were treated as missing characters, and unique synapomorphic nuclear insertions or deletions were indicated on the final trees. These unique indels were considered only when they had clearly defined alignment borders. Each gene was tested for rate heterogeneity among lineages using Tajima's (1993)
relative-rate test. The deer was used as reference taxon each time, and the chi-square probability values were corrected for multiple testing by applying the Bonferroni correction.
In order to test for congruence among genes, the different nuclear DNA segments were analyzed separately using maximum-parsimony and neighbor-joining methods in PAUP, version 4.0b2a, written by David L. Swofford. Due to computational time constraints, no maximum-likelihood analyses were performed for the individual genes. The independent nuclear analyses (Miyamoto and Fitch 1995
) were followed by combined approaches (de Queiroz 1993
), and in this instance, maximum-likelihood analyses were included. Before the data were combined, partition homogeneity tests were performed to identify possible conflicting phylogenetic signals in our data (see also Liu and Miyamoto 1999
). First, the four nuclear DNA segments were tested prior to the generation of a nuclear DNA gene tree. Second, the four nuclear DNA data sets were tested together with the three mtDNA data sets (i.e., seven data partitions) before analyses of the total molecular evidence. In the latter instance, the maximum number of trees saved during each replicate was restricted to 1,000 due to time constraints.
Parsimony analyses utilized 100 replicates of a random taxon addition sequence followed by the heuristic search option with TBR branch swapping. Previous cytochrome b analyses showed that saturation was present at third-codon-position transitions in the cytochrome b gene (Hassanin and Douzery 1999a, 1999b
; Matthee and Robinson 1999
; Rebholz and Harley 1999
), and based on these results, there is seemingly good evidence to exclude these transitions from the analyses. With the exception of this weighting scheme, no differential weighting was used in the present study. However, because removing characters in order to reduce homoplasy does not fundamentally increase general congruence (Vidal and Lecointre 1998
), third-position changes were also included to test for congruence among weighting schemes. Distance and maximum-likelihood analyses were based on the HKY85 (Hasegawa, Kishino, and Yano 1985
) correction, which adjusts for the differences in transition : transversion ratio and also takes into account unequal nucleotide frequencies. Gamma shape parameters were estimated under maximum likelihood for each analysis using the neighbor-joining topology as a starting point. These parameters were included in all of our distance analyses so as to correct for among-sites rate variation.
Nodal support for the parsimony and neighbor-joining analyses was assessed by 1,000 bootstrap iterations, while 100 replicates were performed for maximum-likelihood. For the maximum-likelihood bootstrap analyses, the neighbor-joining tree was used each time as a starting point, and, due to time constraints, the settings for maximum-likelihood did not include among-sites rate variation. Additionally, decay index values (Bremer 1994
) for the nodes were calculated using AutoDecay, version 4.0 (Eriksson 1998
), with default settings. Finally, alternative hypotheses were compared using the Kishino and Hasegawa (1989)
test in PAUP, version 4.0b2a, under maximum likelihood.
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Results and Discussion |
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Sequence Divergence
Based on sequence divergence values, all nuclear DNA segments accumulated changes fairly slowly. The average sequence diversity for the members of the family Bovidae when all nuclear genes were combined was 4.23% (±1.24%), and the divergence values ranged from 0.74% between the lechwe (Kobus lechwe) and the waterbuck (K. ellipsiprymnus) to 6.56% between the Cape grysbok (R. campestris) and the lesser kudu (Tragelaphus imberbis). When the same taxa were compared for the cytochrome b mtDNA gene, the average sequence divergence among taxa was 13.72% (±0.99%); this value roughly translates to a 3.2-fold higher substitution rate in cytochrome b than in the nuclear DNA sequences.
When the nuclear genes were analyzed independently, the Kap-cas segment had the lowest sequence diversity (3.65% ± 1.33%), while the highest was found for the SPTBN1 region (5.03% ± 1.70%). The Thy and PRKC1 genes were intermediate, with average diversities of 3.80% (±1.22%) and 3.93% (±1.63%), respectively. These values clearly reflect different selection constraints on the different genes included in our study. The difference in evolutionary rates among genes is probably best illustrated by the comparison between Thy and SPTBN1, where both gene segments had similar numbers of coding (25%) and noncoding (75%) characters and one (SPTBN1) evolved at least 25% faster than the other (Thy).
Saturation Analyses
From the RI values, it is evident that the nuclear DNA data show little homoplasy (RI = 0.73), while most of the mtDNA characters are homoplastic (RI = 0.45; table 2
). The exclusion of the presumably randomized signal present at third codon positions of cytochrome b (see above) resulted in higher statistical support (bootstrap and decay index values) for the subfamilial clusterings and lower statistical support for the closely related taxa (e.g., within the Alcelaphinae). This is not unexpected given the rate at which phylogenetic signal accumulates coupled with the effects of the randomization of phylogenetic signal over time (Matthee and Robinson 1997, 1999
). Given the focus of the present investigation (subfamilial), we chose to present the bootstrap topology derived from the combined data, where third-codon transitions of cytochrome b were excluded (see below).
Rate Heterogeneity Analyses
Among-sites rate variation was limited in the nuclear DNA data (ranging from 0.765 to 0.938), and, as expected from previous reports, values for the protein-coding cytochrome b gene were much lower (0.480), indicating more among-sites rate heterogeneity for this rapidly evolving protein marker. The proportion of variable sites ranged from 0.08 for the Kap-cas gene to 0.34 for SPTBN1; the mtDNA data had a higher proportion of variable sites (table 2
).
Previous mtDNA studies of bovids which relied on cytochrome b (Matthee and Robinson 1999
) and 12S rRNA gene sequences (Allard et al. 1992
) showed either limited or nonexistent rate heterogeneity among bovid taxa. The nuclear DNA evidence suggested a similar trend. After adjusting P values for multiple testing (2,196 pairwise comparisons in the present nuclear DNA study), there was no significant rate heterogeneity present among the bovid taxa examined.
Independent Gene Analyses
Separate analyses of each gene revealed a high number of most-parsimonious trees (ranging from 29 to 1,950; table 2
). This is primarily the result of terminal polytomies within the monophyletic subfamilies Bovinae, Caprinae, and Alcelaphinae. When the genes were analyzed independently, bootstrapping showed a lack of support for the deeper nodes (defining subfamilies), probably due to the low number of synapomorphies present (65141 for 36 taxa; table 2
). However, all four gene trees consistently supported the distinction between the Bovinae and the other bovid subfamilies, and both equally weighted parsimony and neighbor-joining analyses recovered most subfamilies within the Bovidae with high bootstrap support (fig. 1
). The monophyly of both the Reduncinae and the Cephalophinae was supported by of all four genes, and at least three of four genes supported the monophyly of the remaining five subfamilies as suggested by previous studies (Bovinae, Antilopinae, Hippotraginae, Caprinae, and Alcelaphinae; fig. 1 ). This result is striking given the relatively short nuclear DNA fragments (526854 bp) that were analyzed independently. Both PRKC1 and Kap-cas had <70 parsimony-informative characters (table 2
) for the 36 taxa included, and both fragments recovered at least 10 nodes with bootstrap support >70 when analyzed using parsimony and neighbor-joining analyses (fig. 1
). In sharp contrast, when a collateral comparison was made among the 16S rRNA gene (which has 70 parsimony-informative characters for the same number of taxa; table 2
) and these two nuclear DNA fragments, just four nodes are recovered with bootstrap support >70 (these nodes were those supporting the monophyly of Oryx, Kobus, Redunca, and Raphicerus; data not shown).
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Combined Analyses
Far greater resolution was obtained when the nuclear DNA data set was analyzed without partitioning. The 762 variable and 349 parsimony-informative characters of the combined nuclear analyses (table 2
) supported several previous molecular evolutionary suggestions and also provided new insights into the evolutionary relationships among bovid subfamilies (see below). Tree topologies obtained from maximum-likelihood, parsimony, and neighbor-joining analyses of the complete nuclear DNA data set were largely congruent with that obtained when the mitochondrial and nuclear DNA data were combined (fig. 2
). Although the mtDNA certainly provided additional phylogenetic information, the additional resolution was mostly confined to the tips of the tree (see below). The additional informative characters not only caused an increase in the number of nodes recovered, but also caused an increase in bootstrap support (fig. 1
cf. fig. 2
). Because the choice of outgroup might cause alterations in the ingroup topology (Milinkovitch and Lyons-Weiler 1998
), we also analyzed the nuclear DNA data using midpoint rooting. Apart from slight alterations in the bootstrap support, the main findings of our study remained unaltered.
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Apart from the questionable placement of the suni and the klipspringer, the nuclear DNA data also failed to resolve the phylogenetic position of the impala, giving credence to previous suggestions that the impala should be recognized as a distinct evolutionary lineage, the Aepycerotonidae (Ansell 1971
; Vrba 1979
; Gentry 1992
). Moreover, the average nuclear DNA sequence divergence values separating the three problematical taxa from the remaining bovid subfamilies are larger than or of similar magnitude to the values separating the currently recognized subfamilies (suni = 4.78% ± 0.51%; klipspringer = 3.84% ± 0.62%; impala = 3.99% ± 0.57%). Coupled with the absence of nuclear DNA sequence saturation and the apparent lack of significant rate heterogeneity among lineages, it seems reasonable to argue that the suni, the klipspringer, and the impala are unique species not particularly closely related to any of the recognized bovid tribes/subfamilies. All three are probably older, independent lineages that originated in Africa during the middle Miocene (approximately 15 MYA; Vrba 1985
; Kingdon 1989
).
Resolution Among Bovid Subfamilies
The combined nuclear DNA data proved to be informative in recovering evolutionary relationships among some bovid subfamilies (fig. 2 ). The Bovidae are characterized by a basal division which separates the Bovinae (cow, nilgai, kudu clade) from the remaining bovid taxa. This finding is supported by four unique indels (fig. 2
) and is consistent across independent gene analyses and analytical methods. The bootstrap support for the basal split in the Bovidae tree was 100% in all the combined analyses (fig. 2
), and more than 21 decay steps support each of the two clades as being monophyletic (fig. 3
). Given morphological (Kingdon 1989
), cytogenetic (Buckland and Evens 1978
; Robinson et al. 1998
), and other molecular evidence (Beintema et al. 1986
; Lowenstein 1986
; Gatesy et al. 1997
; Matthee and Robinson 1999
), this finding appears solid and clearly rejects the dental Aegodontia/Boodontia split previously suggested by Schlosser (1904)
.
The central result of the nuclear DNA data was the resolution we obtained within the clade comprising the Alcelaphinae, the Hippotraginae, and the Caprinae (fig. 2
). The combined DNA analyses strongly suggest a close evolutionary link between the African Alcelaphinae and Hippotraginae (one unique indel event; bootstrap support higher than 99% in all instances; and 10 decay steps), and this clade forms a sister assemblage to the more morphologically conservative Caprinae, whose origin might be Eurasian (Vrba 1985
). Furthermore, the maximum-likelihood score of the tree presented in figure 2
is significantly better than the best alternative hypothesis, which does not support the monophyly of this group (t = 2.76; P = 0.0057). This proposal enjoys varying paleontological support. Gentry (1990)
noted that the Alcelaphinae and Hippotraginae share 26 out of 112 selected morphological characteristics, leading him to conclude that Hippotragini are more closely associated with the Alcelaphini than any other bovid tribe. However, he is also of the opinion that the link between the Caprinae and the African antelope is weak. The caprids are characterized by a combination of symplesiomorphic morphological characters (Gentry 1992
), and in spite of previous mtDNA studies, the evolutionary placement of the Caprinae had remained enigmatic (Gatesy et al. 1997
; Hassanin and Douzery 1999a
; Matthee and Robinson 1999
).
The Caprinae notwithstanding, the tribe Reduncini (herein referred to as the subfamily Reduncinae) is the most difficult group to place among the bovid tribes on morphological grounds (Gentry 1992
). They differ morphologically from the Hippotragini (herein referred to as the Hippotraginae) and share many plesiomorphic morphological features with several members of the Bovinae. Although there is some molecular support from both nuclear (see PRKC1 in fig. 1
in the present study and Hassanin and Douzery [1999b
]) and mtDNA cytochrome b sequences (Hassanin and Douzery 1999a
) to suggest that the Reduncinae form part of an assemblage comprising the Caprinae, the Hippotraginae, and the Alcelaphinae, a definitive statement on the group's phylogenetic position is precluded by inconsistencies in topologies, weak bootstrap support, and low decay index values.
The phylogenetic placement of the Antilopinae and the Cephalophinae, together with the problematic suni, impala, and klipspringer (see above), was not a consistent finding in our investigation. Considerable instability occurred among these taxa when the nuclear genes were analyzed separately, and this phenomenon was reflected by the polytomy found in the combined analyses (fig. 2
). As with earlier palaeontological, morphological, and molecular analyses (Vrba 1985
; Lowenstein 1986
; Kingdon 1989
; Georgiadis, Kat, and Oketch 1990
; Gentry 1992
; Modi, Gallagher, and Womack 1996
; Gatesy et al. 1997
; Robinson et al. 1998
; Hassanin and Douzery 1999a
; Matthee and Robinson 1999
), the polytomy of the parsimony tree (fig. 2
) and the short internal branches of the maximum-likelihood tree (fig. 3 ) suggest a rapid radiation within the Bovidae, possibly during the Miocene (Vrba 1985
).
Bovidae Evolution
The outcome of this study, in conjunction with conclusions from previous molecular (Gatesy et al. 1997
; Matthee and Robinson 1999
; Matthee et al. 2001
), morphological, and paleontological studies (Vrba 1985
; Kingdon 1989
; Gentry 1992
), have significantly improved our understanding of bovid evolution. It has been suggested that the antelope lineages became separated from the main Asian boselaphine/bovine lineage near the Oligocene/Miocene boundary approximately 23 MYA (Kingdon 1989
). This early radiation could have resulted from climatic adaptations and/or continental separation of populations (Kingdon 1989
).
Based on the fossil evidence, it is not clear whether the Antilopinae originated in Eurasia or sub-Saharan Africa (Vrba 1985
). Petrified remains reveal that the Antilopinae and the Caprinae were present in Africa near 14 MYA, with Vrba (1985)
suggesting that these two evolutionary lineages probably originated in Eurasia at a much earlier date (also see Kingdon 1989
; Gentry 1992
). Wells (1957)
stated that fossil remains of the Reduncinae are unrecorded in the African Pliocene record, and the only remains predating 10 MYA (which are vaguely related to this group) are found in India. More recently, Vrba (1985)
speculated that the group either originated in Africa during the late Miocene or immigrated from Eurasia. If the molecular association between the Reduncinae and the Caprinae holds, the data at hand would support a Eurasian origin for both the Reduncinae and the Caprinae. The ancestral stock of these lineages probably immigrated into Africa, where they developed into the highly specialized grassland antelopes now represented by the contemporary Reduncinae, Alcelaphinae, and Hippotraginae (Vrba 1985
).
It is noteworthy that the average sequence divergence of 3.68% (±0.32%) between the African tragelaphines (kudu, eland) and the other bovine tribes (buffalo, cow, and nilgai) approximates the 4.14% (±0.54%) average sequence divergence value separating the four mainly African lineages (impala, suni, klipspringer, Cephalophinae) and the Reduncinae/Caprinae/Hippotraginae/Alcelaphinae clade. If the molecular data hold, it seems reasonable that the early diversification of the Bovidae was followed by an African immigration of diverse members belonging to both of the major bovid lineages (Bovinae and a larger "mainly African clade"). Kingdon (1989)
has speculated that the larger Eurasian boselaphines adapted to moister habitats in Eurasia, and the ancestral antelope (represented by the smaller eotragine/neotragines) adapted to drier habitats, making their radiation into Africa possible. It follows that the immigration of the Bovidae into Africa was accompanied by rapid secondary adaptations to open habitats, causing numerous speciation events. The rapid speciation events are clearly corroborated by the short internal branches found in this study (fig. 3
) and, once again, the similarity in sequence divergence distances among most of the subfamilial evolutionary lineages. From these values, it would seem that the African endemics (impala, suni, klipspringer, duikers) originated in Africa at more or less the same time as the first Eurasian immigrations occurred, and these taxa thus represent most likely ancient survivors of the initial bovid radiation in Africa.
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Acknowledgements |
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Footnotes |
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1 Keywords: Bovidae
systematics
nuclear DNA
evolution
phylogeny
2 Address for correspondence and reprints: Conrad A. Matthee, Department of Zoology, University of Stellenbosch, Private Bag X1, Matieland, 7602, South Africa. E-mail: cam{at}maties.sun.ac.za
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