African Elephant Genetics: Enigmas and Anomalies†

Journal of Genetics (2019) 98:83 © Indian Academy of Sciences https://doi.org/10.1007/s12041-019-1125-y PERSPECTIVES African elephant genetics: enigmas and anomalies† ALFRED L. ROCA1,2∗ 1Department of Animal Sciences, and 2Carl R. Woese Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA *E-mail: [email protected]. Received 5 November 2018; revised 28 March 2019; accepted 27 May 2019 Keywords. elephants; mito-nuclear; subspecies; effective population size; glacial refugia. During the last two decades, our understanding of the Introduction genetics of African elephant populations has greatly increased. Strong evidence, both morphological and genetic, sup- Morphological analyses of skull dimensions of African ele- ports recognition of two African elephant species: the phants from widespread locations in Africa have revealed savanna elephant (Loxodonta africana) and the forest ele- complete separation morphologically between forest and phant (L. cyclotis). Among elephantids, phylogeographic savanna elephants, with a few intermediaries primarily patterns for mitochondrial DNA are highly incongruent with in habitat transition zones (Groves and Grubb 2000a, b; those detected using nuclear DNA markers, and this incon- Grubb et al. 2000). Various nuclear genetic studies have gruence is almost certainly due to strongly male-biased gene also reported that forest and savanna elephants are genet- flow in elephants. As our understanding of elephant popula- ically distinct and deeply divergent (Roca et al. 2001; tion genetics has grown, a number of observations may be Comstock et al. 2002; Rohland et al. 2010; Palkopoulou considered enigmatic or anomalous. Here, several of these et al. 2018), with a limited degree of ongoing hybridization are discussed. (i) There are a number of within-species mor- between the two species (Roca et al. 2001; Comstock et al. phological differences purported to exist among elephants 2002; Mondol et al. 2015). Genetic polymorphisms includ- in different geographic regions, which would be difficult to ing indels (insertion-deletion variants) that are common reconcile with the low genetic differentiation among popula- in one species may be completely or almost completely tions. (ii) Forest elephants have a higher effective population absent from the other, further demonstrating the lack of size than savanna elephants, with nuclear genetic markers nuclear gene flow between forest and savanna elephants much more diverse in the forest elephants than savanna ele- (figure 1)(Roca et al. 2001). Hybrid elephants near the for- phants, yet this finding would need to be reconciled with the est edge carry genetic markers typical of both species, yet life history of the two species. (iii) The savanna and forest the genetic variants in ones species do not introgress into elephants hybridize and produce fertile offspring, yet full- the other species (figure 1)(Roca et al. 2001, 2005), empha- genome analysis of individuals distant from the hybrid zone sizing the genetic isolation of savanna elephants from suggests that gene flow has been effectively sterilized for at forest elephants, and strongly supporting their status as least ∼500,000 years. (iv) There are unexplored potential distinct species (Mayr 1942, 1963, 1969; Roca et al. 2001, ramifications of the unusual mito–nuclear patterns among 2005, 2007). This separation is also supported by differ- elephants. These questions are considered in light of high ences in behaviour and life history traits (Grubb et al. 2000; male and low female dispersal in elephants, higher variance Turkalo et al. 2017, 2018). Further, millions of years of of reproductive success among males than females, and of genetic divergence separate forest and savanna elephants, a habitat changes driven by glacial cycles and human activity. separation almost as deep as that between Asian elephants (Elephas maximus) and woolly mammoths (Mammuthus †This is one of the articles of collections on ’Conservation Genetics’. primigenius)(Rohland et al. 2010; Palkopoulou et al. 2018). 0123456789().: V,-vol 83 Page 2 of 12 Alfred L. Roca Figure 1. Differences in the phylogeographic patterns of nuclear and mitochondrial markers among forest and savanna elephants. Sets of pie charts indicates for each locality the frequencies of species-typical genetic markers including: maternally-inherited mtDNA (left), paternally-inherited Y chromosome (right) or biparentally-inherited markers (centre). In each pie chart, the green colour indicates markers within clades typical of forest elephants (including mitochondrial ‘F clade’), while the blue colour indicates markers within clades typical of savanna elephants (including mitochondrial ‘S clade’). Total indicate the number of individuals (for mtDNA, Y chromosomes) or combined number of chromosome segments (biparentally inherited markers) examined. At locales with an asterisk, the number of forest-typical and savanna-typical markers was significantly different (P < 0.05) between mtDNA and biparentally inherited markers. Inset beneath the map are the expected pattern for a recent hybrid (left), while the term ‘conplastic’ is more typically used for laboratory mice in which mtDNA from one strain is bred into a second strain by backcrossing hybrid females to males only from the second strain (Yu et al. 2009). This pattern is analogous to those found in localities in which savanna elephants carry mtDNA derived from forest elephants, but show no evidence of forest elephant nuclear gene introgression, and implies a similar pattern of backcrossing. The biparentally inherited markers are three unlinked X-chromosome intronic segments; similar patterns are present in diploid autosomal markers (Roca et al. 2001; Ishida et al. 2011, 2013; Mondol et al. 2015). Forest localities: DS, Dzanga Sangha; LO, Lope; OD, Odzala. Savanna localities: AB, Aberdares; AM, Amboseli; BE, Benoue; CH, Chobe; HW, Hwange; KE, central Kenya; KR, Kruger; MA, Mashatu; MK, Mount Kenya; NA, Namibia; NG, Ngorongoro; SA, Savuti; SE, Serengeti; SW, Sengwa; TA, Tarangire; WA, Waza; ZZ, Zambezi. Garamba (GR) is in a transition zone of vegetation in Congo that includes both habitats and both elephant species (White 1983; Groves and Grubb 2000a, b). Dark green is tropical forest habitat; light green is the forest-savanna transition zone of vegetation (White 1983). Figure is from my own publication which permits reuse of figures with this reference to the original publication (Roca et al. 2005). Analyses of nuclear genomes indicate that the forest O’Brien 2005). In many cases of interspecies hybridization, and savanna elephants have been genetically isolated for mitochondrial but not nuclear DNA crosses the species at least 500,000 years. By contrast, mtDNA patterns barrier when females are the nondispersing sex (Petit and show frequent introgression of forest elephant mtDNA Excoffier 2009). in savanna elephant populations (figure 1)(Eggert et al. As the number of elephant population genetic studies 2002; Nyakaana et al. 2002; Debruyne 2005; Johnson has increased, a number of findings have been reported et al. 2007; Ishida et al. 2011, 2013). Male elephants dis- that appear to be anomalous or enigmatic. Those that perse from their natal social group, while females do not may be considered anomalous appear at first glance to (Douglas-Hamilton 1972; Moss 2001). Thus, unlike all the be inconsistent with what may be expected, especially in other genetic markers for which gene flow can be medi- light of other known aspects of elephant biology. Others ated by males, there is little gene flow for mtDNA due may be considered enigmatic because they are puzzling to nondispersal of females that remain with core social or difficult to explain, often because there may not be groups (Ishida et al. 2011). The discordant mtDNA pat- enough information to infer strong conclusions about terns detected in elephants are thus attributable to sex the causes or consequences of some facet of elephant differences in dispersal (Roca et al. 2005, 2007; Roca and genetics. This article considers several different aspects of African elephant genetics Page 3 of 12 83 elephant genetics that may be considered to fall into these categories. Regional morphological differences within African elephant species are purported to exist, although within-species genetic differentiation is low There are a number of reputed geographic differences in the morphology of forest and of savanna elephants within their respective species ranges. For example, the desert dwelling elephants of Namibia are said to be taller and leaner, with longer legs and larger feet than other populations of savanna elephants, and they have been proposed as a distinct subspecies (Ishida et al. 2018). Several taxa of pygmy elephants have been said to inhabit the tropical forests of Africa (Frade 1955; Groves and Grubb 2000a, b; Debruyne et al. 2003). Other regional differences have been reported among both forest and savanna elephants, with over 20 subspecies proposed, largely based on purported morphological differences (Frade 1955). Reports of geographic differences in the morphology of different populations of African elephants are difficult to reconcile with genetic data. Among savanna elephants, male dispersal and gene flow are quite high, and this would Figure 2. Genetic differentiation is low within forest and within tend to limit the degree of genetic differentiation among savanna elephants. Forest and savanna elephants are distinct populations of savanna

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