Reconciling apparent conflicts between mitochondrial and nuclear phylogenies in African elephants.

Yasuko Ishida,Sergios-Orestis Kolokotronis,Kai Zhao,Alfred L. Roca,Victor A. David,Nicholas J. Georgiadis,William J. Murphy,Taras K. Oleksyk,Robert M. Stephens

doi:10.1371/journal.pone.0020642

Abstract

Conservation strategies for African elephants would be advanced by resolution of conflicting claims that they comprise one, two, three or four taxonomic groups, and by development of genetic markers that establish more incisively the provenance of confiscated ivory. We addressed these related issues by genotyping 555 elephants from across Africa with microsatellite markers, developing a method to identify those loci most effective at geographic assignment of elephants (or their ivory), and conducting novel analyses of continent-wide datasets of mitochondrial DNA. Results showed that nuclear genetic diversity was partitioned into two clusters, corresponding to African forest elephants (99.5% Cluster-1) and African savanna elephants (99.4% Cluster-2). Hybrid individuals were rare. In a comparison of basal forest “F” and savanna “S” mtDNA clade distributions to nuclear DNA partitions, forest elephant nuclear genotypes occurred only in populations in which S clade mtDNA was absent, suggesting that nuclear partitioning corresponds to the presence or absence of S clade mtDNA. We reanalyzed African elephant mtDNA sequences from 81 locales spanning the continent and discovered that S clade mtDNA was completely absent among elephants at all 30 sampled tropical forest locales. The distribution of savanna nuclear DNA and S clade mtDNA corresponded closely to range boundaries traditionally ascribed to the savanna elephant species based on habitat and morphology. Further, a reanalysis of nuclear genetic assignment results suggested that West African elephants do not comprise a distinct third species. Finally, we show that some DNA markers will be more useful than others for determining the geographic origins of illegal ivory. These findings resolve the apparent incongruence between mtDNA and nuclear genetic patterns that has confounded the taxonomy of African elephants, affirm the limitations of using mtDNA patterns to infer elephant systematics or population structure, and strongly support the existence of two elephant species in Africa.

Highlights

Central to the successful management of endangered taxa is determination of whether their populations comprise one or more species
Samples recently collected included forest elephants from the Bili Forest in the Democratic Republic of Congo, a location previously not included in elephant genetic studies; and a forest elephant sample from the Paris Zoo (France) of Sierra Leone origin (Figure 1) [29]
The lack of gene flow between forest and savanna populations, despite the existence of a hybrid zone, has especially supported their status as species under the biological species concept [46,47,48]: among 1764 savanna elephant X-chromosome sequences previously examined, 1762 (99.9%) had been found to be haplotypes not present among forest elephants, while not a single savanna elephant nuclear haplotype has ever been reported in a tropical forest elephant population [4]

Summary

Introduction

Central to the successful management of endangered taxa is determination of whether their populations comprise one or more species. Recent studies have renewed debate about their taxonomy, after both morphological and nuclear DNA analyses suggested that African elephants form two distinct species separated by a relatively narrow hybrid zone [1]. Skull measurements from 295 elephants of known provenance suggested that forest and savanna elephants fall into two morphologically distinct species [2,3]. Nuclear DNA analyses using both slower-evolving nuclear sequences [4,5,6] and more rapidly evolving microsatellite loci [7] have provided concordant evidence that forest and savanna elephants are distinct species [4,6,8,9] that are as divergent genetically as Asian elephants are from mammoths [5]. Few morphological intermediates [3,10] and nuclear genetic hybrids [4,6,7] between forest and savanna elephants have been detected, primarily in a zone of mixed forest-savanna habitat that surrounds the tropical forests of Africa [1]

Methods

Results

Conclusion