Article in press - uncorrected proof Mammalia 72 (2008): 2–14 ᮊ 2008 by Walter de Gruyter • Berlin • New York. DOI 10.1515/MAMM.2008.004 Review Afrotherian mammals: a review of current data Rodolphe Tabuce1,*, Robert J. Asher2 and Introduction Thomas Lehmann3 1 Institut des Sciences de l’Evolution, cc064, The resolution of the phylogenetic relationships among Universite´ Montpellier II, place Euge` ne Bataillon, mammalian placental orders and the question of when 34095 Montpellier cedex 05, France, and where the eutherian radiation took place is a contro- e-mail: [email protected] versial topic between morphologists (including paleon- 2 Department of Zoology, University of Cambridge, tologists) and molecular biologists. Molecular analyses, Downing Street, Cambridge CB2 3EJ, UK based on large nuclear gene datasets strongly support 3 Museum fu¨ r Naturkunde der Humboldt-Universita¨t zu the division of living placental lineages into four superor- Berlin, Forschungsabteilung Invalidenstrasse 43, dinal groups: Afrotheria, Xenarthra, Euarchontoglires and 10115 Berlin, Germany Laurasiatheria (Murphy et al. 2001a,b, Scally et al. 2001, Amrine-Madsen et al. 2003, Springer et al. 2004, Niko- *Corresponding author laev et al. 2007, Nishihara et al. 2007, Springer and Murphy 2007, Wildman et al. 2007) (Figure 1). The clade Afrotheria includes six placental orders: Proboscidea Abstract (elephants), Sirenia (dugongs and manatees), Hyracoidea (hyracoids), Macroscelidea (elephant-shrews), Tubuliden- The supraordinal mammalian clade Afrotheria was first tata (aardvarks) and Tenrecoidea (tenrecs and golden recognized in its entirety based on DNA analysis dating moles, also known as ‘‘Afrosoricida’’). According to these to the mid-1990s. Since then, this ‘‘African clade’’, which analyses, these taxa evolved and have been in Africa includes proboscideans, sirenians, hyracoids, tubuliden- since the Cretaceous. tates, elephant-shrews, tenrecs and chrysochlorids, has Compared to the overwhelming molecular and geno- been supported by numerous molecular and genomic mic support for Afrotheria (Redi et al. 2007, Springer and studies. According to these molecular inferences, the ori- Murphy 2007), the available morphological data are gin of crown Afrotheria goes back into the Cretaceous, equivocal concerning the validity of such a clade. The with estimates from over 100 to under 80 Mya. Morpho- different Afrotherian orders have long been scattered logical phylogenies have not completely recovered Afro- among ungulates (proboscideans, sirenians, hyracoids theria, although its paenungulate core (proboscideans, and tubulidentates), lipotyphlan insectivores (tenrecids sirenians and hyracoids) was named in 1945 by the pale- and chrysochlorids), or considered as the sister group of ontologist George Simpson. Recent paleontological glires (macroscelids). One explanation for this disagree- studies concur with molecular ones in evoking some ment between molecules and morphology is the sup- affinities between paenungulates, aardvarks and ele- posed long endemic evolution of afrotherians that may phant-shrews. Moreover, the position of tenrecs and have overwritten morphological afrotherian synapomor- golden moles within afrotherians is supported by some phies (Robinson and Seiffert 2004). According to the fos- recent concatenations of morphological and molecular sil record, afrotherians have indeed a long history on the phylogenetic datasets. The phylogenetic position of Afro- Afro-Arabian continent. Likewise, their living representa- theria relative to the other supraordinal placental clades has been debated, the most recent analyses of genomic tives are mostly present in Afro-Arabia and Madagascar, and concatenated data support a basal position within except for the Asian elephant, West Indian and Amazo- Placentalia. Molecular data suggest an African origin for nian manatees, and Australasian dugongs. The study of Afrotheria and a long period of endemism on that conti- the earliest afrotherians, and eutherians in general, is nent. When adding the paleontological data to this sce- thus important because they provide direct evidence of nario, the paleobiogeographic history of Afrotheria the order of acquisition of characters. These fossils pres- becomes more complex. For instance, these data argue ent character combinations absent in modern taxa, and for the broad distribution of afrotherians during the Ter- they allow the study of characters that have been tiary and do not exclude their Laurasian origin. In fact, ‘‘erased’’ by subsequent evolution within a clade (Benton some Laurasian taxa could be closely related to the ear- 1995). liest afrotherians (hyracoids, proboscideans and ele- In that regard, the recent studies of such fossil euthe- phant-shrews) found in the early Eocene of North Africa. rians on one hand (Zack et al. 2005, Tabuce et al. 2007, Other Afrotherian groups are known with certitude from Wible et al. 2007), and the mapping of several morpho- East Africa since the beginning of the Miocene. logical characters observed on living afrotherians on molecular phylogenies on the other hand (Werdelin and Keywords: fossil record; molecules; morphology; Nilsonne 1999, Whidden 2002, Cox 2006, Mess and phylogeny. Carter 2006, Sa´ nchez-Villagra et al. 2007) have revealed 2007/4 Article in press - uncorrected proof R. Tabuce et al.: Review of Afrotheria 3 Figure 1 Phylogeny of Afrotheria defined by nuclear and mitochondrial DNA sequence data based on a consensus of recent phylogenetic analyses (Kjer and Honeycutt 2007, Springer and Murphy 2007). Known stratigraphic distribution of afrotherian orders are indicated by black bold lines. Question mark indicates the possible occurrence of stem and/or crown Afrosoricida (tenrecs plus golden moles) during the Paleogene (Seiffert et al. 2007). some interesting characters proposed as afrotherian from the late Eocene of Dor el Talha, Libya (Mahboubi et synapomorphies. al. 1986, Court 1995). Proboscidean features of Numi- In this paper, we summarize the fossil record of early dotherium are the pneumatized skull and the second inci- afrotherians, review the strong molecular signal for Afro- sors enlarged as tusks. Recently, O’Leary et al. (2006) theria and synthesize the morphological data relative to reported an indeterminate proboscidean from the Eocene afrotherian monophyly focusing on recent advances. We of Mali. Other Paleogene genera (Moeritherium, Barythe- also consider the latest large morphological datasets and rium, Phiomia and Palaeomastodon) are well document- the combined molecular-morphological analyses that ed in the rich beds of the late Eocene to early Oligocene deal with interordinal mammalian relationships in order to layers of the Fayum, Egypt (Andrews 1906) and from oth- discuss the group’s African origin, their divergence times er parts of Arabo-Africa (Shoshani et al. 1996). Moerithe- and their supposed long Afro-Arabian endemism. rium was long considered morphotypic for the order, but it is now considered as a peculiar early offshoot within proboscideans (Delmer et al. 2006). Phiomia and Palaeo- Fossil record of early afrotherians mastodon are considered more closely related to modern elephants (elephantoids) than other Paleogene taxa Proboscidea according to their columnar limbs, large tusks, external nasal opening shifted in front of the orbits, etc. (Tassy The oldest and most primitive proboscidean is Phospha- 1996). Recently, primitive deinotheres and gomphotheres therium from the earliest Eocene of Ouled Abdoun basin, have been discovered in the late Oligocene of Ethiopia, Morocco (Gheerbrant et al. 1996, 1998, 2005a) (Figure extending the fossil records of these more modern 2). This fox-sized genus is known by several jaws and groups considerably back in time (Sanders et al. 2004). partial skulls. Although plesiomorphic in its anterior den- The first Asian elephantoid is known from the early tition and skull structure (‘‘condylarth’’-like), Phosphathe- Oligocene of Pakistan (Antoine et al. 2003). rium is typically proboscidean by its true lophodonty and the orbit opening in the maxilla. Daouitherium, also from Sirenia the Ypresian of Morocco, shares with Phosphatherium numerous dental traits (Gheerbrant et al. 2002). Daoui- Sirenia is the only taxon of the clade Afrotheria to have therium appears to be structurally intermediate between fossils on most continents (except Antarctica) (Figure 3). Phosphatherium and Numidotherium, a genus known The oldest and most primitive fossil record for Sirenia is from the early to middle Eocene of El Kohol, Algeria and Prorastomus, a member of the family ‘‘Prorastomidae’’, Article in press - uncorrected proof 4 R. Tabuce et al.: Review of Afrotheria Figure 2 Phylogeny of early proboscidean taxa showing stratigraphic and geographic distributions. Question marks indicate uncer- tain phylogenetic relationships (modified from Gheerbrant et al. 2005b). found in the early middle Eocene of Jamaica (Savage et air sinuses, and dense and swollen ribs (Gheerbrant et al. 1994). This animal is only known by a skull, mandible al. 2005b). From these taxa, Gheerbrant et al. (2005b, p. and atlas. Therefore, the earliest ascertained fully quad- 88) extracted some basal sirenian traits: ‘‘premaxilla-fron- rupedal sirenian is Pezosiren, a slightly younger taxon tal contact, enlarged premaxillary rostrum with slightly also found in Jamaica and included in the ‘‘Prorastomi- enlarged I1, long, deep, and narrow mandibular symphy- dae’’, but represented by abundant