Mitochondrial DNA phylogeography of red deer (Cervus elaphus)

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Abstract

In order to understand the origin, phylogeny, and phylogeography of the species Cervus elaphus, we examined the DNA sequence variation of the mitochondrial cytochrome b gene of 51 populations of deer from the entire distribution area of Cervinae with an emphasis on Europe and Asia. Several methods, including maximum parsimony, maximum likelihood, and nested clade analysis, revealed that red deer originated from the area between Kyrgyzstan and Northern India. We found two distinct groups of red deer: a western group consisting of four subgroups and an eastern group consisting of three subgroups. Our mtDNA data do not support the traditional classification of red deer as only one species nor its division into numerous subspecies. The discrepancies between the geographical pattern of differentiation based on mtDNA cytochrome b and the existing specific and subspecific taxonomy based on morphology are discussed.

Introduction

Red deer (Cervus elaphus) is the most widespread and best known deer species in the world. Today there are up to 22 known subspecies (Table 4) in the Holarctic (Geist, 1999; Trense, 1989; Whitehead, 1972). Although much is known about the phylogeny of the species (Geist, 1999; Kuwayama and Ozawa, 2000; Mahmut et al., 2002; Polziehn and Strobeck, 1998, Polziehn and Strobeck, 2002; Randi et al., 1998, Randi et al., 2001; Trense, 1989), there are still some disagreements. Whereas the division into the two species C. elaphus and Cervus canadensis is widely accepted (Bryant and Maser, 1982; Cockerill, 1984), their subdivision into many subspecies is questioned (Cronin, 1992; Nowack, 1991) as is the assignment of the Central Asian subspecies to the two lineages elaphus and canadensis (Geist, 1999; Polziehn and Strobeck, 2002; Mahmut et al., 2002; Trense, 1989). Since cladistic analyses detected many cases of parallelism and convergence in the evolution of morphological traits among Cervidae (Groves and Grubb, 1987; Janis and Scott, 1987), the understanding of their pattern of character evolution requires the drawing of a phylogeny independent from those traits (Randi et al., 1998). The present classification of the numerous subspecies is mostly based on morphological characters such as body and antler size (Dolan, 1988), antler shape (e.g., coronate or acoronate) or cranial measurements (Geist, 1991, Geist, 1992) which are all considerably affected by nutrition (Geist, 1999). Recent morphological studies have concentrated more on nutrition-independent characters such as the hair coat of social organs, social signals (Geist, 1999) and postcranial measurements (Pfeiffer, 2002). These studies as well as the most recent studies on mitochondrial DNA (Mahmut et al., 2002; Polziehn and Strobeck, 2002; Randi et al., 2001) query the number of subspecies and favor the classification of red deer into two different species. The mitochondrial protein-coding gene for cytochrome b has been proven to be useful for resolving phylogenetic patterns among various artiodactyls within evolutionary time frames shorter than 25 million years (Stanley et al., 1994; Tanaka et al., 1996).

In this study we analyzed the phylogeny of 50 populations of most living species and subspecies of the genus Cervus by comparing complete mtDNA cytochrome b sequences. The aim of this study was to answer the following questions: Does the red deer represent only one species (C. elaphus) with numerous subspecies distributed all over the Holarctic (Geist, 1999; Whitehead, 1972), or are there two different species (C. elaphus and C. canadensis) consisting of an eastern and a western group (Kuwayama and Ozawa, 2000; Mahmut et al., 2002; Polziehn and Strobeck, 1998, Polziehn and Strobeck, 2002; Randi et al., 1998, Randi et al., 2001)? Do the currently named subspecies agree with phylogenetic and phylogeographic knowledge based on genetic data? Does the origin of C. elaphus lie in Central Asia as has been assumed by Geist (1999) and Mahmut et al. (2002)? We also discuss the paths of distribution of this widespread species.

Section snippets

Sample collection and laboratory procedures

Samples of tissue or antlers were obtained from 37 wild populations of red deer (C. elaphus) across most of the species range (Fig. 1), with 1–15 individuals from each population being sampled (Table 1). Additional three sequences of red deer were obtained from the NCBI nucleotide data bank for comparison and verification of our data. The following species were included in the study to determine species status: Sika deer (Cervus nippon) with five different subspecies (four from the NCBI

Characterization of sequence variation

A total of 52 (eight from the NCBI nucleotide data bank; Accession Nos. AB021092–AB021096, AB021098, AB021099, and AJ000022) out of 125 mitochondrial cytochrome b sequences (1140 nucleotides each), representing 51 populations, 45 haplotypes and 30 Cervinae taxa (according to Geist’s (1999) classification), were included in the calculation (Table 1). Sequence identity was observed only among individuals originating from the same or adjacent geographical regions but for all individuals from the

Species or not species?

The phylogenetic trees obtained from the sequence data from the cytochrome b gene of mtDNA, support the classification of Western Red Deer and Eastern Red Deer as individual species. The integration of sika deer and Thorold’s white lipped deer as sister taxa in the phylogenetic analysis clearly identify Western and Eastern Red Deer as two monophyletic groups (Fig. 2). The fallow deer (D. dama) showed a distance between 0.111 and 0.126 to the examined groups. This confirms the state of Dama as a

Conclusion

Sequence deviation and the difference in the mtDNA cytochrome b gene in the various groups of the genus Cervus, appears to be informative and may be used as a marker to describe species boundaries, to appoint subspecies and to find the geographical origin of unidentified samples. Due to our results the present classification of red deer into a large number of subspecies has to be reconceived. This study shows a very high probability for the existence of two different species of red deer with

Acknowledgements

We thank C. Oswald for providing us with rare samples which in some cases are difficult to achieve. We thank T. Pfeiffer for assistance in palaeontological questions. Further thanks are extended to J. Bissonette and U. Puszkarz for helpful comments on this manuscript. Financial support of the Deutsche Forschungsgemeinschaft (DFG) is gratefully acknowledged.

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