Antelope Evolution

Antelope is a term used to refer to several ungulate species within the Bovidae GRAY 1821 family, from the sub-order Ruminantia SCOPOLI 1777, order Artiodactyla OWEN1848. They share many anatomical and behavioural characteristics, playing a central role in the nutrient cycling of the ecosystems they inhabit, where they shape the vegetation cover through herbivory and secondary seed dispersal, and are preyed by large carnivores (Hassanin et al. 2012; Bro-Jørgensen 2016). The classification of sub-families and tribes within the Bovidae is still debatable, with some alternatives proposed.

Nevertheless, 88 antelope species exist today, classified into almost 30 different genera, most of which are native to Africa (Hassanin et al. 2012; Bro-Jørgensen 2016).

1.2.1 Shared characteristics

All antelopes share several behavioural and morphological adaptations that are taxonomically diagnostic (Brashares, Garland and Arcese 2000). They have hooves, meaning the tip of their toes is covered by a keratin cover that grows continuously (Prothero 1993; DeMiguel, Azanza and Morales 2014). Also, they have specialized and well-developed molar teeth, with a consequent reduction or even absence of canine and incisor teeth (Mendoza and Palmqvist 2008). Both sexes have bony cranial appendages (horns), which grow continuously. The horn size and shape vary greatly among species, but horns are always unbranched and have a bony core covered by a permanent sheet of keratin (Prothero, 1993; DeMiguel et al. 2014). All antelopes are even-toed ungulates, meaning that they bear there weight equally on the central two toes (Matthee et al. 2001).

Also, as ruminants, all antelopes are able to digest pant-based matter in a four-chambered stomach (Matthee et al. 2001; Hume 2002). Most antelopes are mixed

feeders, browsing and grazing, according to seasonal availability of each plant type (Pérez-Barbería, Gordon and Illius 2001). Other shared morphological characteristics include a blunt-end snout, pointing ears, and long tail (Figure 1.6).

Figure 1. 6 Examples of African antelope species. A) giant eland (Taurotragus derbianus), photo by David Mallon (IUCN);

B) royal antelope (Neotragus pygmaeus), copyright Harry Kouwer (britannica.com); C) Thompson’s gazelle (Eudorcas thomsonii), photo by Yathin S. Krishnappa; D) addax (Addax nasomaculatus), photo by Jeff Kigma/Alamy (britannica.com); E) impala (Aepyceros melampus), photo by Frans Lanting (franslanting.photoshelter.com); and F) gemsbok (Oryx gazelle), copyright Carl Landsberg (treknature.com).

Antelopes vary greatly in size, both in height and weight. The smallest antelope species is the royal antelope (Neotragus pygmaeus), measuring 25 cm tall and weighing about 3 kg, whereas the largest one is the giant eland (Taurotragus derbianus), with a full mature male reaching 180 cm at the withers and weighing up to 1,000 kg. Most African antelopes have medium to large-sized bodies and present a clear sexual dimorphism, with larger and heavier males (Weckerly 1998; Loison et al. 1999; Pérez-Barbería, Gordon and Pagel 2002). Coat colouration ranges from pale white (as in the Addax – Addax nasomaculatus) to black (as in the sable antelope – Hippotragus niger), but intermediate brownish or reddish tones are more common. Across several species, sexual dichromatism leads to light-coloured coat across females and young males (Stoner, Caro and Graham 2003). Camouflage is also an important adaptation since all

species are prey for carnivores (Nokelainen and Stevens 2016). Among antelopes, it can manifest as prominent or faint stripes (as in the greater kudu – Tragelaphus strepsiceros), strong facial markings to hide the prominent eyes (as in gazelles – Gazella spp.), as well as blending body patterns (as in impala – Aepyceros melampus) or, on the contrary, strong contrasting colour patterns (as in the gemsbok – Oryx gazella), to conceal it from the background and confuse predators (Stoner et al. 2003). Most African antelopes are gregarious and territorial. Groups have a strong social structure, generally consisting of a territorial male and a variable number of females and juveniles. When males become sexually mature, they are forced to disperse into new territories, and fight other males for dominance, using their horns (Bro-Jørgensen 2011). Females probably developed their horns for defence against predators or express territoriality (Estes 1991;

Stankowich and Caro 2009).

1.2.2 Phylogenetic context

Combining molecular, morphological, and fossil information obtained across several studies, Fernández and Vrba (2005) obtained a well-supported phylogenetic supertree for Ruminantia. Within Ruminantia, Bovidae constitutes a monophyletic family with at least nine sub-families. Incomplete fossil record, extensive morphological convergence, and a rapid radiation within Bovidae has led to taxonomic inconsistencies at the sub-familial level (Allard et al. 1992; Janecek et al. 1996; Hassanin and Douzery 1999;

Matthee and Davis 2001). Nevertheless, two main clades have consistently been retrieved, comprising of the Bovinae and remaining taxa. Bibi (2013) and Hassanin et al.

(2012) were able to retrieve concordant phylogenetic relationships analysing whole-mitochondrial data of extant Bovidae taxa. Recent genomic data corroborates previous reconstructions, while improving sub-familial inconsistencies (Chen et al. 2019) (Figure 1.7). Divergence time estimations across both the mitochondrial and nuclear genomes, together with fossil calibrations, agree with a general view of a bovid radiation during the Miocene through the Pliocene period. Estimated divergence time between Bovinae and non-Bovinae taxa is about 16 Mya, for both the nuclear and mitochondrial genome (95%

CI 15.1-17.3 Mya; Bibi 2013; Chen et al. 2019).

The Bovinae clade includes the African buffalo (Syncerus caffer), and several African antelope species such as the greater kudu (Tragelaphus strepsiceros) and the giant eland (Taurotragus derbianus). The non-bovine clade also contains non-antelope African bovids, such as the wildebeest (Connochaetes spp.), as well as savanna-adapted antelopes, such as the Thompson’s gazelle (Eudorcas thomsonii), the impala (Aepyceros melampus), and the hartebeest (Alcelaphus buselaphus). The Hippotraginae

sub-family comprises of antelope species only, from three different genera. Two of them – Addax and Oryx – include desert or semi-desert adapted-species. The first includes a single species, the addax (Addax nasomaculatus), distributed across the Sahara Desert.

Orix genus contains four species: the East African oryx (O. beisa), across the Somalian region; the scimitar oryx (O. dammah), widespread throughout the Sahara; the gemsbok (O. gazella), distributed throughout arid regions of Southern Africa and the Kalahari Desert; and the Arabian oryx (O. leucoryx), restricted to the Arabian Peninsula. The third genus, Hippotragus, contains two extant savanna-adapted species: the roan (H.

equinus) and the sable antelope (H. niger). This genus will constitute the main focus of this thesis. The node corresponding to Hippotraginae sub-family is estimated between 6.6 Mya, according to the mitogenome (95% CI 5.6-7.6 Mya; Bibi 2013), and around 8 Mya, according to the nuclear genome (Chen et al. 2019).

Figure 1. 7 Schematic cladogram showing intra-familial phylogenetic relationships within Bovidae family, adapted from Chen et al. (2019). Nodes are identified according to main genera composing them, and on the right is shown the corresponding sub-family.

1.2.3 African expansion

The first bovid-like fossil belongs to the extinct genus Eotragus and dates back to the Miocene, around 23 Mya (Vrba 1996; Bibi 2009). Because it was found in both France and sub-Saharan Africa, the common ancestor to all African antelopes is attributed to a species which either, extended its distribution, or was capable of long-distance migrations between continents (Matthee and Davis 2001; Bibi 2011; Moorley and Kingdon 2013). Based on the fossil record, it is also likely that Antilopinae, Reduncinae, and Capridae originated in Eurasia and subsequently expanded into Africa, around 10 to 14 Mya (Vrba 1996; Fernández and Vrba 2005). The earliest antelope-like fossil is from a member of the Antilopinae (Pseudoeotragus seegrabensis) found in Austria, estimated to be 17 to 18 million years. However, fossils attributed to the current Gazelle genus date back to the late mid-Miocene, around 14 Mya, across Kenya (Bibi 2009). This is coincident with the estimated divergence time for the Antilopinae node across the nuclear and mitochondrial genome of about 14 Mya (95% CI of 13.6-15.8 Mya; Bibi 2013;

Chen et al. 2019). The oldest African records of Reduncinae were found in Chad and Kenya, and are dated to 8 Mya (Bibi 2009), which is consistent with an estimated divergence time of 7.1 Mya, from mitogenomic analysis (95% CI 6.3-8.0 Mya; Bibi 2013).

The nuclear genome phylogeny, however, suggests an older ancestor for this sub-family, around 13 Mya (Chen et al. 2019). This period between the Miocene-Pliocene boundary, corresponds further with the earliest fossil records for Alcelaphinae (Kenya, 6.5-7.5 Mya), Hippotraginae (Chad, 7 Mya), and Tragelaphinae (Kenya, 5.7-6.7 Mya) (Bibi 2009).

Subsequent divisions within each sub-family and across genera occurred throughout the Pliocene (~2.5 to 5 Mya) and Pleistocene (~100 kya to 2.5 Mya) periods (Bibi 2013).

The mid-Pliocene African climatic shift towards cooler temperatures and increased aridity, corresponds with widespread fossil record of grazing mammals and adaptation towards grasslands and savannas (Vrba 1996; Dupont, 2011; Bibi and Kiessling 2015).

Across several paleontological deposits in East and South Africa, the characterization of faunal communities, through both species abundance and dietary isotopic measures, demonstrates an elevated turnover rate between 2 and 3 Mya (Bobe and Eck 2001; Bobe and Behrensmeyer 2004; Kingston and Harrison 2007; Faith and Behrensmeyer 2013).

Analysis of bovid fossils along a geological timeline clearly shows a shift in species abundance from primarily browsers, associated with closed and wetter habitats (e.g Reduncinae), towards the ones that have a grazing nature, occurring mostly across more open and drier conditions (e.g Hippotraginae). Modern Hippotraginae species, for example, are primarily obligate grazers, distributed across desert grasslands and open woodlands. However, dietary isotopic measures across the Laetoli deposits, in northern

Tanzania, indicate that these species might have been mixed feeders or even primarily browsers during the Pliocene (between 3.5 and 3.8 Mya) (Kingston and Harrison 2007).

Records at the same site from 2.5 to 2.7 Mya, show a tendency towards mixed foraging strategies, not only across Hippotraginae, but generally for bovid specimens. Studies like this show that, even though bovid evolution during this period can be largely attributed to a global climate shift, local environmental changes can shed light on complex biotic interactions at smaller scales (Bibi and Kiessling 2015).

1.2.4 Pleistocene refugia

As previously stated, Pleistocene climatic and vegetational changes shifted the range and variety of existing biogeographical regions across sub-Saharan Africa, and therefore, the spatial distribution of biological groups. How these climatic cycles influenced range expansions of taxa became a topic of interest (Hewitt 1996, 1999, 2000;

Taberlet et al. 1998). The onset of phylogeography, by combining phylogenetic data on extant taxa with geographic and climatic history, allowed us to further understand how past events shaped current spatial patterns and genetic diversity (Avise 2009). Even though most studies were biased towards temperate biota across higher latitudes (Beheregaray 2008), several were performed across African savanna mammals (e.g.

elephant; Nyakaana, Arctander and Siegismund 2002), including bovine (e.g. buffalo;

van Hooft, Groen and Prins 2002) and antelope species (e.g. hartebeest, topi and wildebeest; Arctander, Johansen and Coutellec-Vreto 1999; kob antelope; Birungi and Arctander 2000; impala and greater kudu; Nersting and Arctander 2001).

By performing a comparative analysis across several phylogeographic studies on taxa with overlapping distributional ranges, it is possible to infer common patterns of spatial genetic discontinuities (Bermingham and Moritz 1998; Arbogast and Kenagy 2001).

Hewitt (2004) compiled several phylogeographic studies on African savanna mammals to get some insight on how Pleistocene climatic cycles influenced their population structure, divergence, and diversity. Savanna habitats were prevalent across the continent throughout mid-Pleistocene, with high abundance around 1.2 and 1.7 Mya, and increasing prevalence towards late-Pleistocene, from 600 kya (Hewitt 2004). Also according to the author, divisions at the species level seem to be very recent and occurred mostly in the last 400 kya. Based on divergence level between clades, Hewitt (2004) identified three main areas across sub-Saharan Africa that consistently encompassed major divergences within species: West, East, and South (Figure 1.8).

Phylogenetic analyses, patterns of population structure, and diversity measures, indicated that these three main regions most likely acted as refugia for savanna-adapted

taxa during moist pluvials. from where surviving populations would expand during subsequent drier interpluvials (Hewitt 2004). During these favourable periods, several re-colonisations between these main regions would occur, creating contact zones of previously isolated populations, with increased diversity (Hewitt 2001, 2011).

Figure 1. 8 Geographic location of main Pleistocene pluvial refuge areas for African mammals, adapted from Hewitt (2004) and Lorenzen et al. (2012): West (in green); South (in purple); South-West (in red); as well as East (in blue) acting as contact zone between the former. Black double-sided arrows depict range expansion movements during interpluvials.

Also represented is the East African Rift System – EARS, adapted from Chorowicz (2005). Major faults are depicted in black curves, representing the eastern and western branches, as well as minor faults, in black dotted curves, namely the Eastern Arc Mountains – EAM. Land cover is represented from forests (in green) to mountains (in brown), with shaded relief, depicting higher altitude.

The continued publication of phylogeographic studies on African mammals made this pattern of Pleistocene refugia more apparent, especially among ungulate species strongly associated with the savanna biome, such as the giraffe (Brown et al. 2007), the roan antelope (Matthee and Robinson 1999; Alpers et al. 2004), and the sable antelope (Pitra et al. 2002, 2006). By combining their own work with available data on these species, Lorenzen and co-workers (2012) performed a robust comparative phylogeographic analysis. Across 19 ungulate species, 13 of which were antelopes, they validated Hewitt’s proposal on Pleistocene refugia across West and South Africa, suggesting a second refugium in Southern Africa, centred in the southwest, for certain species (e.g. the sable antelope). They also suggested that East Africa acted mainly as

a contact zone during interpluvial range expansions, presenting itself as a mosaic of smaller refugia, with higher overall diversity levels. The complex pattern in East Africa was mostly driven by high species turnover, exacerbated by habitat instability associated with the continued volcanic and tectonic activity of the EARS (Trauth et al. 2009; Moorley and Kingdon 2013). The Pleistocene refuge theory thus postulates that the maintenance of non-forestry refugia during pluvials enabled the persistence of species through repeated glacial cycles. These patches of suitable habitat promoted the divergence between refuge populations during periods of isolation, as well as the accumulation of genetic diversity due to species' persistence. Range expansion rates during interpluvials and the presence of geomorphological barriers, dictated the position of contact zones, and ultimately shaped the spatial patterns that we see today across African taxa, namely savanna-adapted antelope species (Lorenzen et al. 2012).