The African savannah biome harbours an ungulate (hoofed mammal, see Box 1) community of unique diversity. The diversity exceeds that of any other biogeographic region, even when accounting for the Late Pleistocene megafauna extinctions of Eurasia and America (Owen-Smith & Cumming 1993). The savannah biome spans the tropical grasslands, scrublands and wooded savannahs of sub-Saharan Africa, encompassing the Sahel—the vast semi-arid region of North Africa south of the Sahara, the Rift Valley formation in equatorial East Africa and most of Southern Africa (Fig. 1) (Mayaux et al. 2004). It is punctuated by the extended tropical forests of Central and Western Africa and the fragmented coastal forests of Eastern Africa (Mayaux et al. 2004; de Vivo & Carmignotto 2004). The distribution and biomass density of ungulates is clearly associated with the distribution of savannah habitat (Fig. 2a) (du Toit & Cumming 1999), and many herbivores prefer areas of low tree density: a top-down response to minimize risks of predation (Riginos & Grace 2008).
|Although it bears no taxonomic significance, the term ungulate is used in a descriptive sense to refer to any mammal with hooves. The taxonomy of African ungulates has been a subject of intense debate (e.g. Simpson 1945; Gentry 1992; Fernández & Vrba 2005; Wilson & Reeder 2005), which is expected, given the unique diversity of the assemblage. Traditionally, species were identified and distinguished based on morphology (e.g. coat colour, size, craniometry), behaviour and ecology. This resulted in a very high number of described taxa (e.g. Christy 1924; Ruxton & Schwarz 1929), and as in other areas of systematics, the multitude of proposed species concepts has led to a dichotomy of the two polarized approaches to species delimitations: lumping and splitting.|
|With the advent of molecular genetics, the evolutionary relationships between populations within species have been investigated using genetic markers, and genetic data have been used to identify taxonomic units. In several cases, studies based on mtDNA and microsatellites have revealed a discrepancy between genetic diversity and morphological variation, for example kob (Lorenzen et al. 2007a), Grant’s gazelle (Lorenzen et al. 2007b), and zebra (Lorenzen et al. 2008), suggesting that either method alone is a poor proxy for taxonomic inference.|
|The World Conservation Union (IUCN 2011) currently recognizes 92 antelope species worldwide. A recent review on ungulate taxonomy has increased this number substantially to 204 by lifting many local ecotypes and subspecies to full species status (Groves & Grubb 2011). For example, the Alcelaphine taxa included in our review have been split into several species: hartebeest into eight, wildebeest into four and topi into 11. While we do not discuss the validity of the approach used by Groves & Grubb (2011), where fixed differences in any character such as morphology, behaviour or genetic variation are used to define a species, we have not followed their species delimitations.|
|Rather, we have applied a pragmatic approach and have treated as species those taxa that were treated as such in the reviewed studies, unless subsequent genetic-based research has shown this to be erroneous. Some species complexes have therefore been lumped, for example Grant’s gazelle and giraffe. Others such as bushbuck and African elephant, a dominant member of the herbivore assemblage, have been omitted, as the available phylogeographic studies on these taxa have in hindsight proven difficult to interpret. In the only phylogeographic study of bushbuck to date, it was treated as a monophyletic group (Moodley & Bruford 2007). However, it consists of two species, and perhaps even two species complexes, which are paraphyletic with respect to the other tragelaphines (Moodley et al. 2009). Recent genetic data have convincingly shown that African elephant consists of two distinct species: forest and savannah (Ishida et al. 2011). To date, there has been no phylogeographic study of savannah elephant—the species of relevance here—without the inclusion of its sister species, which complicates the inference of intraspecific diversity.|
Around 80% of ungulates belong to the bovid family, which includes the true antelopes and buffalo (du Toit & Cumming 1999). The emergence and evolutionary success of the group is closely linked to the increased dominance of grassland formations on the African continent (Kappelman et al. 1997; Bobe & Behrensmeyer 2004; Edwards et al. 2010). Data from marine records indicate that African climates shifted towards cooler temperatures and greater aridity at the onset of the Pleistocene c. 2.8 million years (Ma) ago (deMenocal 1995). Soil carbonate and n-alkane carbon isotopes document the progressive expansion of xeric vegetation around this time, including woodland and grassland savannahs (Feakins et al. 2005). The long-term increase in open habitats and arid-adapted C4 plants facilitated the emergence of species with an associated diet (deMenocal 2004), and many bovid taxa first appeared in the fossil record c. 2.8 Ma ago (Vrba 1995; Bobe et al. 2002; Bobe & Behrensmeyer 2004).
Owing to changes in the Earth’s orbital forcing parameters, African climates became increasingly variable during the Pleistocene (deMenocal 1995; Maslin 2007; Trauth et al. 2009). Climate forcing mechanisms operated at both global scales—such as the glacial cycles of the northern hemisphere (deMenocal 1995)—and local scales, for example insolation-driven monsoons (Trauth et al. 2009) and the progressive formation of the Rift Valley in East Africa (Trauth et al. 2007).
The physiography of sub-Saharan Africa varies, but for convenience and as far as the distribution of wide-ranging species are concerned, the region can be divided into two major vegetation zones: savannah and tropical forests (Fig. 1; Lehmann et al. 2011). The distributional balance between the two is governed by precipitation (Lehmann et al. 2011; Staver et al. 2011). Climate variability in tropical Africa during the Pleistocene mainly resulted in changes in levels of precipitation, with oscillations between warm, wet periods (pluvials) and cooler periods of reduced humidity (interpluvials) (Dupont 2011). Pollen records from marine sediments covering several Pleistocene glacial–interglacial cycles indicate the repeated expansion and contraction of savannah and forests (Dupont 2011). During dry interpluvials, the decrease of CO2 and precipitation facilitated an increase in savannah coverage; southern hemisphere grasslands shifted northward and West African savannahs expanded at the cost of lowland forests (Dupont 2011). During moist pluvials, the scenario reversed and grasslands were replaced by expanding tropical forests (Cowling et al. 2008).
Ungulate population sizes are intrinsically linked with climate change over evolutionary timescales (Lorenzen et al. 2011), and the distributions of savannah herbivores would have shifted in accordance with vegetation change. When climates change and habitats are altered, species are forced to adapt, migrate or go extinct. The Pleistocene refuge theory (Haffer 1969) was originally conceptualized for Neotropical rain forests, but can equally be applied to the African savannahs. The maintenance of isolated grassland refugia—core areas of stable savannah habitat—during moist pluvials would have enabled the continued survival of savannah-adapted taxa. Over time, natural selection and genetic drift would promote the divergence of species genomes, ultimately shaping differences between populations in behaviour, morphology and ecology (Avise 2000).
Biogeographic insights from genetic data
Phylogeography is the study of the geographic distribution of genetic lineages (Avise 2000). In combination with population genetic inference, it provides a powerful approach to elucidating the evolutionary processes that have shaped present-day diversity within and among species. Comparative phylogeography uses data from taxa with varying life history traits, habitat preferences and ecological requirements to elucidate the historical biogeography of a region (Moritz 1998). As hypothesized in models of environmentally driven evolution (Vrba 1995), congruent phylogeographic patterns across taxonomic groups and trophic levels suggest similar forces shaped species evolutionary histories.
Most comparative phylogeographic studies have been focused on northern temperate zones, owing to the accumulation of data from especially Europe and North America (see references in Shafer et al. 2010). There have been few comparative works from the southern hemisphere and tropical regions. Within the past two decades, phylogeographic studies have been published on two-dozen ungulate taxa from sub-Saharan Africa. With the rapid accumulation of data from large-scale studies, the time is ripe to synthesize the work and summarize the overall findings.
In this review, we explore data from 19 ungulate taxa for which region- and continent-wide data exist. The taxa are ecologically associated with savannah ecosystems, although each has unique habitat preferences and life history traits (Estes 1991). Most of the taxa included are medium-sized and large bovids, reflecting the predominance of the group within the herbivore guild. We focus on major biogeographic signals within each taxon and evaluate community-wide patterns in the context of Pleistocene climate change.