New Phylogenetic Analysis of the Family Elephantidae Based on Cranial-Dental Morphology.код для вставкиСкачать
THE ANATOMICAL RECORD 293:74–90 (2010) New Phylogenetic Analysis of the Family Elephantidae Based on Cranial-Dental Morphology NANCY E. TODD* Department of Biology, Manhattanville College, Purchase, New York ABSTRACT In 1973, Vincent Maglio published a seminal monograph on the evolution of the Elephantidae, in which he revised and condensed the 100þ species named by Henry Fairﬁeld Osborn in 1931. Michel Beden further revised the African Elephantidae in 1979, but little systematic work has been done on the family since this publication. With addition of new specimens and species and revisions of chronology, a new analysis of the phylogeny and systematics of this family is warranted. A new, descriptive character dataset was generated from studies of modern elephants for use with fossil species. Parallel evolution in cranial and dental characters in all three lineages of elephants creates homoplastic noise in cladistic analysis, but new inferences about evolutionary relationships are possible. In this analysis, early Loxodonta and early African Mammuthus are virtually indistinguishable in dental morphology. The Elephas lineage is not monophyletic, and results from this analysis suggest multiple migration events out of Africa into Eurasia, and possibly back into Africa. New insight into the origin of the three lineages is also proposed, with Stegotetrabelodon leading to the Mammuthus lineage, and Primelephas as the ancestor of Loxodonta and Elephas. These new results suggest a much more complex picture of elephantid origins, evolution, and paleogeography. C 2009 Wiley-Liss, Inc. Anat Rec, 293:74–90, 2010. V Key words: elephant; evolution; cladistics In 1973, Vincent Maglio published a seminal monograph on the evolution of the Elephantidae. In his phylogeny, three lineages of elephants, Loxodonta, Elephas, and Mammuthus, evolved from Primelephas in Africa, 6 ma. Not only did Maglio (1973) summarize the origin, evolution, and zoogeography of the entire family, he also consolidated the 100þ species proposed by Henry Fairﬁeld Osborn in his two-volume Proboscidea into 25 valid species. Beden (1979) expanded on Maglio’s (1973) work, but focused on the African Elephantidae. He was responsible for the identiﬁcation and description of material from East Lake Turkana, Kenya, the Omo Valley, Ethiopia, Laetoli, Tanzania, and Hadar, Ethiopia. These collections represent the bulk of the elephant material from Africa, and his collected works are a testimony to the effort and required to identify such a large amount of material in such a small amount of time. In 1996, The Proboscidea, The Evolution and Palaeoecology of Elephants and Their Relatives (Shoshani and Tassy, 1996) was published as an update of proboscidean C 2009 WILEY-LISS, INC. V studies since Osborn’s 1936 and 1942 Proboscidea volumes. Seventeen other species have been added to the list of taxa recognized by Maglio (1973). Some were considered to be junior synonyms by Maglio, but have now been re-evaluated and reinstated. Others are completely new species. Since 1996, three additional species have been described and a number of subspecies are now formally recognized. This brings the total number of elephantid species to 43, though not all of these are included in the cladistic analysis presented in this article (Table 1). This article is dedicated in the memory of Dr. Jeheskel Shoshani. *Correspondence to: Nancy E. Todd, Department of Biology, Manhattanville College, 2900 Purchase Street, Purchase, NY 10577. Fax: (914)323-5121. E-mail: firstname.lastname@example.org Received 16 August 2008; Accepted 25 June 2009 DOI 10.1002/ar.21010 Published online in Wiley InterScience (www.interscience.wiley. com). 75 PHYLOGENETIC ANALYSIS OF THE ELEPHANTIDAE TABLE 1. Current classiﬁcation of the family elephantidae [after Shoshani and Tassy (1996)] Maglio (1970) Shoshani and Tassy (1996) Additional species/subspecies Stegotetrabelodon syrticus Stegotetrabelodon orbus Stegotetrabelodon lybicus Stegotetrabelodon exoletus Stegodibelodon schneideri Primelephas gomphotheroides Primelephas korotorensis Loxodonta adaurora Loxodonta Loxodonta Loxodonta Loxodonta Loxodonta Loxodonta Loxodonta atlantica Loxodonta africana Loxodonta exoptataa Elephas ekorensis Elephas recki Stages I-IV Elephas iolensis Elephas namadicusb Elephas falconeric Elephas Elephas Elephas Elephas Elephas Elephas Elephas Elephas Elephas Elephas Elephas Elephas Elephas Elephas Elephas (Paleoloxodon) (Paleoloxodon) (Paleoloxodon) (Paleoloxodon) (Paleoloxodon) ? beyeri (Paleoloxodon) (Paleoloxodon) meletensis brumptia shungurensisa atavusa ileretensisa reckia Elephas Elephas Elephas Elephas Elephas recki recki recki recki recki Elephas Elephas Elephas Elephas maximus maximus maximus indicus maximus sumatranus nawatensis antiquus falconeri mnaidriensis creutzburgi naumanni creticus cypriotes planifrons celebensis platycephalus hysudricus hysudrindicus maximus Mammuthus subplanifrons Mammuthus africanavus Mammuthus meridionalis Laiatico Stage, Montavarchi Stage, and Bacton Stage Mammuthus armeniacusd Mammuthus primigenius Mammuthus colombie Mammuthus imperator adaurora adauroraa adaurora kararaea atlantica atlanticaa atlantica zulu africana africana africana cyclotis Mammuthus meridionalis gromovi Mammuthus meridionalis meridionalis Mammuthus meridionalis vestinus Mammuthus trogontherii Mammuthus? jeffersoni Mammuthus exilus Mammuthus hayi Mammuthus lamarmorae # Species 25 40 Mammuthus rumanus 43 a Named by Michel Beden. E. antiquus ¼ junior synonym. c Maglio felt that Elephas mnaidriensis (Adams, 1870), Elephas meletensis (Falconer and Cautley, 1862, 1868), Elephas lamamorae (See Mammuthus) (Major, 1883), Elephas cypriotes (Bate, 1903), and Elephas creticus (Bate, 1907) were successive stages in dwarﬁng and perhaps did not warrant species designations. d M. trogontherii ¼ junior synonym. e M. jeffersoni ¼ junior synonym. b Both Maglio’s (1973) and Beden’s (1979) monographs were primarily concerned with specimen and species identiﬁcation. Character evolution was determined by identifying an ancestor from the older fossils from which the evolution of more recent elephants could be deduced. The material recovered from late Miocene and early Pliocene African localities seemed to be the key to the origin of the family. Preoccupation with an ancestral morphotype, and the progressive development of characters from this morphotype to the extant elephants has 76 TODD resulted in a preoccupation with anagenetic trends. Subsequent to Maglio (1973), species and subspecies have been deﬁned based on their position within these trends, rather than based on the morphological characteristics that they share or do not share with other species. As a result, traditional systematic methods have been unable to distinguish between homoplasies (which occur in parallel in all lineages of elephants), plesiomorphies, and synapomorphies. Unfortunately, this emphasis on identiﬁcation led to inconsistent use of terminology, character descriptions, and measurement methods. Many of the similarities in morphology among fossil elephants were based on plesiomorphic characters. Loxodonta has long been thought to represent the ancestral condition for the family, and yet many similarities have been observed between this genus and several late Pleistocene taxa in Europe (Todd, 1997). Unrelated species were grouped together based on superﬁcial resemblances that were the result of parallel evolution or retention of ancestral characters (Maglio 1973). This is further complicated by the widespread parallel evolution that has occurred in all three lineages, Elephas, Mammuthus, and Loxodonta. There have been few attempts to examine the relationships of species within the Elephantinae through character-based analysis. Tassy (1988, 1990), Tassy and Darlu (1986, 1987), and Kalb and Mebrate (1993) have examined the Order Proboscidea and/or the Suborder Elephantoidea using cladistic methods. Tassy (1988, 1990) and Tassy and Darlu (1986, 1987) have analyzed the relationships within the Proboscidea, particularly the relationships of tetralophodont-grade elephantoids to each other and to the Elephantidae. In his discussion of phylogeny and classiﬁcation of the Proboscidea, Tassy (1990) reviews previous classiﬁcations and examines the relationships within the order using parsimony. His cladogram of the Proboscidea is resolved except for node 13 (the Elephantoidea deﬁned as including the Mammutidae, Ambelodontidae, ‘‘gomphotheres,’’ Choerolophodon, Stegodontidae, and the Elephantidae). This is the crucial node for the origin of the elephantines (Stegodibelodon, Primelephas, Loxodonta, Mammuthus, and Elephas), and suggests that the origin of the Elephantidae is not as simple as may have been previously thought. Previous research has been aimed at determining the probable ancestor of the family Elephantidae, the relationships of the sister groups Stegodontidae and Gomphotheriidae to the Elephantidae, and the status of the paraphyletic ‘‘gomphothere’’ group. As a result, many of the characters used in these analyses are too generalized to distinguish between species within the Elephantidae. The Elephantidae are included in these analyses at the generic level only, and no study of the species relationships within the family has been done. Kalb and Mebrate (1993) analyzed characters at the generic level in African elephants, using proboscidean specimens from the Middle Awash, Ethiopia. This is the only recent study which focuses on dental characters of African Elephantidae using character-based analysis. They separate a ‘‘Loxodonta Group’’ from Loxodonta adaurora and discuss the relationships of both Loxodonta clades to a Primelephas-Mammuthus-Elephas clade. They grouped Primelephas with Mammuthus and Elephas based on synapomorphies (concave-concave enamel loops on lower molars, single posterior column). Twin posterior columns in Loxodonta adaurora and convex-concave enamel loops in the Loxodonta Group separate these two groups from the Primelephas-Mammuthus-Elephas clade (Kalb and Mebrate, 1993). The presence of a prominent posterior column which is completely isolated in unworn molars in these species reﬂects the ancestral ‘‘trefoil’’ pattern from a gomphothere ancestor, and thus explains the direction of the development of the median loop (Kalb and Mebrate, 1993). Study of the morphology of the extant species (Loxodonta africana and Elephas maximus) provides the basis for a more rigorous analysis of the characters used to deﬁne fossil species and subspecies of Elephas, Loxodonta and potentially Mammuthus (Todd, 2009). The goal of this article is to present a cladistic analysis of the Elephantidae based on a new, descriptive cranialdental character dataset, and to suggest a new phylogenetic scheme for the family. MATERIALS AND METHODS Species and Specimens Because of the variability in specimens that have been assigned to fossil taxa in the Elephantidae, and the variability in descriptions of such taxa in the literature, characters were coded on the type specimens for each species and subspecies only. The type specimen data is proposed as the most accurate representation of the ‘‘true’’ morphology of each fossil and modern species. Most of the type specimens consist of molars only, but some do include the cranium and/or mandible. In a few cases, only the mandible and mandibular teeth exist. A few of the type specimens do not exist anymore, or the specimen was inaccessible. The whereabouts of the type for Loxodonta africana (originally named Elephas africanus) is unknown. This specimen was examined using a drawing from Osborn (1942:1197), and another molar from the type locality (Cape Colony) located in the British Museum of Natural History. The only designated type for any of the subspecies of Loxodonta africana or Elephas maximus is ‘‘Congo,’’ the type specimen for Loxodonta africana cyclotis. This specimen was located in the American Museum of Natural History. An adult representative of each of the other extant subspecies was chosen as the specimen for use in coding character states. The types for Loxodonta atlantica and Elephas iolensis are housed in the Musée Nationale d’Histoire Naturelle in Paris, but are listed without specimen numbers. These are ﬁgured in Osborn (1942), however, and the type localities for each are listed. The molars best matching both of these were examined during research in Paris. An excellent cast of the type for Mammuthus subplanifrons was examined in the British Museum. Only one specimen of Mammuthus meridionalis was studied, and this was used as the example for this species. The lectotype for Loxodonta exoptata is from Laetoli, Tanzania, and is housed in the Humboldt Universität, Berlin. This specimen is ﬁgured by Maglio (1969:18, Plate I, Figs. 1 and 2), and the photograph was used in addition to a specimen from East Turkana, Kenya. The lectotype for Elephas recki (also Elephas recki recki) is from Olduvai Gorge, Tanzania and is located in the same museum. The specimen itself was not examined, but a cast reconstruction matching the ﬁgure from Osborn (1942) that was in the collections of the National PHYLOGENETIC ANALYSIS OF THE ELEPHANTIDAE Fig. 1. Ordered analysis of cranial, dental, and mandible characters with successive weighting produced one cladogram in which the Asian elephant groups with E. antiquus and the rest of the Eurasian Elephas, while the African elephant occupies a position closer to the basal African fossil species. A Nelson Consensus Tree of the 16 unordered trees remains largely unresolved. The genera are color coded, with the African Elephas is in blue, and the Eurasian Elephas in light blue. Stegotetrabelodon the outgroup. Museum of Kenya was studied. The types for the subspecies Elephas recki brumpti, and Elephas recki shungurensis are from the Omo Valley, Ethiopia, and were not available for study. Figures of these from Beden (1979) and comparable specimens from other collections were used as the example for each. The type for Elephas recki atavus is on display in the Gallerie de Paléontologie in Paris. This is a very complete cranium with both upper third molars still in place. The mandible for Elephas recki atavus was not found, and so KNM-ER 5711 was used for mandibular characters. This specimen consists of a cranium and mandible that is virtually identical to the type specimen. The type specimen for Elephas ekorensis consists of upper right and left M3, and so cranial data was collected from KNM-EK 422, a partial cranium housed in the National Museums of Kenya. A list of the type specimens and specimens used to code for characters is included in Table 2. Cladistic Analysis Data sets were analyzed using Hennig86. With the exception of one analysis, trees were obtained using the mhennig command with branch swapping (mh*; bb*) (trees were obtained for one dataset using ie*). For each data set, trees were obtained from ordered, successively weighted characters (cc; xsteps w) as well as unordered and successively weighted characters (cc-; xsteps w). Finally, multiple trees were condensed into a Nelsen consensus tree (n; tplot). Seventy-seven multistate characters were examined on two species of extant elephants and 15 extinct species. This dataset includes a total of 77 multistate characters: 33 dental characters, 32 cranial characters, and 12 mandible characters deﬁned based on the osteological analysis of the extant elephants, as well as the extinct species (Table 3) (Todd, 1997). Three general skeletal characters and seven phenotypic characters were also studied, but at the present time, these can only be used 77 Fig. 2. Unordered analysis of cranial, dental, and mandible characters with successive weighting produced 16 cladograms. A Nelson Consensus Tree of the 16 unordered trees remains largely unresolved. The genera are color coded. African Elephas is in blue, and the Eurasian Elephas in light blue. to identify subspecies of the two living elephants and so are not included in the cladistic analysis. RESULTS Once the character set was established, the literature was surveyed in detail for comparison of character descriptions. This was necessary to insure consistent terminology. Previous studies by Maglio (1973) and Beden (1979, 1983, 1987) provided the groundwork for interpreting differing descriptions, but these descriptions are often not used consistently across taxa. This has made it difﬁcult to compare species and specimens, and is the principle reason for developing a new, well-deﬁned character data set. Many of the new characters have a foundation in these previous studies, but all are new in terms of their descriptions and states. Two examples of the comparison process between previous studies and the new analysis are the dental characters involving folding of the enamel and the shape of the enamel ﬁgure. Enamel folding is so variable in fossil elephants that it was necessary to separate this general character into ﬁve separate characters. The basic trend in dentition that has been proposed for all elephant lineages is increased shearing efﬁciency of the molars. This was accomplished in different ways in each lineage, but there are allometric and functional changes in several features which are intricately related. To increase plate spacing while maintaining numbers of plates, the enamel thickness had to decrease. To compensate for thinner (and less durable) enamel, the crown height increased. To compensate for thinner enamel, and maintain adequate surface area, enamel became increasingly folded. Although the degree and type of enamel folding varies among species, there are very deﬁnite characteristics which can be isolated as characters with several states each. Enamel folding is so complicated in fossil elephants, that not only the pattern was coded but also four additional characters were created: placement of folds, amplitude of folds, spacing of enamel folds, and crenated versus smooth enamel. Every specimen was coded for these characters, and the results show a high degree of 78 TODD TABLE 2. Type specimens and specimens substituted for types in this analysis Species Stegotetrabelodon orbus Primelephas gomphotheroides Loxodonta adaurora and Loxodonta adaurora adaurora Loxodonta adaurora kararae Loxodonta atlantica Loxodonta africana Loxodonta africana oxyotis Loxodonta africana cyclotis Loxodonta exoptata Elephas ekorensis Elephas recki and E. r. recki Elephas recki brumpti Elephas recki shungurensis Elephas recki atavus Elephas recki ileretensis Elephas iolensis Elephas antiquus Elephas namadicus Elephas hysudricus Elephas meletensis Elephas mnaidriensis Elephas maximus maximus Elephas maximus indicus Elephas maximus sumatranus Mammuthus subplanifrons Mammuthus meridionalis Mammuthus armeniacus Type specimen Comments KNM-LT 354 KNM-LT 351 KNM-KP 385 KNM-ER 347 MNHN Location unknown, type locality probably Cape Colony, ﬁgured in Osborn (1942:1197)a No type specimen AMNH 90102 (?) ‘‘Congo’’ IPUB Z.94.96, ﬁgured in Maglio (1969:18)a KNM-EK 424 IPUB XVII 1382b Omo L1.33, ﬁgured in Beden (1979:387)a Omo 148.72.1, ﬁgured in Beden (1979:397)a MNHN 1933.9.300 KNM-ER 1588 MNHN BM M.2006 BM M.3092 BM M.3109 BM M.44312 BM M.44304 No type specimen No type specimen No type specimen MMK 3020, cast in BMNHb IGF 1054a BM 32250, BM 32252 Partial mandible with LLM2-and LLM3 ULM3, URM3, LM3, and fragmentary palate Almost complete adult skeleton, partial cranium with UM3, and complete mandible with LM3 Partial cranium with UM3 Co-type, LRM2, 1 referred specimen-ULM3 LRM2, used URM3 from Cape Colony locality, and NMNH 304615 for cranium and mandible characters Used NMNH 304615 Complete cranium and mandible M2 in wear and M3 forming LRM3, also used KNM-ER 3200 A-B URM3, ULM3, also used KNM-EK 422 (cranium) LLM2 in mandible fragment, examined cast of this specimen Mandible fragment with LLM2 and LLM3 Maxilla fragment with ULMa and ULM3 Complete cranium with URM3 and ULM3 Maxilla fragment with URMb and URMa LLM3 LLM2 Partial cranium with frag. UM3 Cranium ULMa(?) LRM3 Used ROM 01.2.8.1 Used AMNH 30249 Used NMNH 282837 Type of ‘‘Archidiskodon subplanifrons’’ Used MNHN 1948-1-126 ULM3 and URM3, also referred to ‘‘M. trogontherii’’ a A cast of this specimen was examined. These specimens were not examined during the course of this study, but drawings and photographs were used to code for characters, as well as other comparable specimens. b polymorphism within-species. Even when separated into ﬁve different multistate characters, there is still a wide range of variation. A second example of comparisons with previous studies and the new analysis is the shape of the enamel ﬁgure. Again, the descriptions of this feature in the literature are varied and too comprehensive for it to be a single character. As described in the introduction, some of this variation is due to developmental plasticity, but is also related to shape changes in the molars, such as overall width and allometric changes in enamel and plate thickness. In this case, the original feature has been divided into six multistate characters: presence of anterior/posterior columns, general enamel ﬁgure shape, shape of median area, lateral edges of enamel ﬁgure, direction of lateral edges of enamel, and symmetry of median loop. As with the ﬁrst example, these characters are still highly polymorphic. Cladistic Analysis The total data set includes 33 dental characters, 32 cranial characters, and 12 mandibular characters. The outgroup, Stegotetrabelodon orbus, and nine other species are included in this analysis. When characters are or- dered, one tree was obtained with a Length ¼ 176, CI ¼ 65, and RI ¼ 51 (Fig. 1). When the characters are unordered, 16 equally parsimonious trees are obtained with Length ¼ 153, CI ¼ 71, and RI ¼ 53. A Nelson Consensus Tree is represented in Figure 2. The overall structure of the two ﬁnal trees is the same, though the relationship of Eurasian Elephas to African Elephas is unresolved. The dental data set contains 33 dental characters. The outgroup is Stegodon kaisensis and includes 18 other species. As this data set is based only on dentition, more species can be included. Stegodon kaisensis (Stegodontidae) is a member of the sister group to the Elephantidae, and provides a better outgroup than Stegotetrabelodon when all genera of the Elephantidae are included in the analysis. However, there is no cranial material for Stegodon kaisensis, so it cannot be used as an outgroup in the total character analysis. Nineteen equally parsimonious trees were obtained with the characters ordered, Length ¼ 151, CI ¼ 43, RI ¼ 58. One tree resulted with successive weighting of characters (Fig. 3). In an unordered analysis, two equally parsimonious trees were obtained with a Length ¼ 120, CI ¼ 50, and RI ¼ 60. The only difference between the two trees is the position of S. orbus and P. gomphotheroides (Fig. 4). PHYLOGENETIC ANALYSIS OF THE ELEPHANTIDAE TABLE 3. Cranial, dental, and mandible characters used in the cladistic analysis Dental characters 1. Molar shape 0 ¼ tapered at anterior end (ovate) 1 ¼ parallel-sided 2 ¼ widest in middle (elliptic) 3 ¼ tapered at posterior end (ovate) 2. Molar curvature 0 ¼ straight 1 ¼ curved at posterior end (occlusal view) (occlusal view) 3. Molar shape 0 ¼ height even at both ends 1 ¼ greatest height at posterior end *Generally characterizes upper and lower teeth (lateral view) 4. Greatest tooth width 0 ¼ base of crown 1 ¼ 1/4 up from base of crown 2 ¼ 1/2 up from base of crown 3 ¼ crown (posterior view) 5. Molar crown 0 ¼ ends at alveolar border 1 ¼ extends below alveolar border (lateral view) 6. Cingulum 0 ¼ present 1 ¼ absent (lateral view) 7. Occlusal surface 0 ¼ even 1 ¼ twisted 2 ¼ sagging in middle (posterior 8. Inclination of plates to occlusal surface 0 ¼ weak 1 ¼ strong (lateral 9. Valleys between plates 0 ¼ V-shaped 1 ¼ U-shaped (lateral 10. Valley shape at base 0 ¼ compressed, diverge at apex 1 ¼ parallel (lateral 11. Cement ﬁlling valleys 0 ¼ no 1 ¼ yes view) view) view) view) (lateral view) 12. ‘‘S’’ curve to plates 0 ¼ no 1 ¼ yes (lateral view) 13. Lateral edges of plate 0 ¼ low and rounded 1 ¼ straight, angled in toward apex 2 ¼ parallel-sided 3 ¼ high and bowed out slightly 14. Molar roots 0 ¼ strong or bifurcated 1 ¼ absent or open (posterior view) 79 80 TODD TABLE 3. Cranial, dental, and mandible characters used in the cladistic analysis (continued) Dental characters 15. Apical digitations 0 ¼ few (4 or less) 1 ¼ many (greater than 4) (occlusal view) 16. Appearance of complete enamel loops 0 ¼ slow (within 6 worn plates) 1 ¼ quick (within 3 worn plates) (occlusal view) 17. Single column at posterior end 0 ¼ present 1 ¼ small plate *May be variable (occlusal view) 18. Anterior/Posterior columns 0 ¼ strong anterior column 1 ¼ strong posterior column 2 ¼ strong anterior and posterior columns 3 ¼ no anterior/posterior columns 19. Median cleft 0 ¼ strong 1 ¼ weak 2 ¼ absent 20. Tusk shape 0 ¼ straight 1 ¼ curved or spiralled in front 2 ¼ straight spiral (twisted) 21. Tusk cross-section 0 ¼ rectangular or ﬂattened 1 ¼ oval or ‘‘bean’’ shaped 2 ¼ round 22. Enamel height above cement 0 ¼ Low 1 ¼ High *May be related to wear and amount of abrasion 23. Enamel ﬁgure shape 0 ¼ parallel-sided 1 ¼ true lozenge 2 ¼ parallel-sided with median loop 3 ¼ ‘‘pseudo-lozenge’’ 4 ¼ ‘‘keyhole’’ shaped 5 ¼ rounded loops 24. Median area 0 ¼ loop 1 ¼ fold 2 ¼ absent or open 25. Lateral sides of enamel ﬁgure 0 ¼ pinched 1 ¼ rounded 2 ¼ intermediate 3 ¼ rectangular 26. Direction-lateral sides of enamel 0 ¼ turn anterior 1 ¼ turn posterior 2 ¼ even *May be variable 27. Symmetry of enamel ﬁgure 0 ¼ symmetrical, in line with long axis of molar 1 ¼ asymmetrical, offset from long axis of molar PHYLOGENETIC ANALYSIS OF THE ELEPHANTIDAE TABLE 3. Cranial, dental, and mandible characters used in the cladistic analysis (continued) Dental characters 28. Medial edges of enamel ﬁgures 0 ¼ separated 1 ¼ in contact 29. Enamel folding 0 ¼ absent 1 ¼ regular 2 ¼ irregular 3 ¼ undulating 4 ¼ crinkled 30. Placement of folds 0 ¼ median area only 1 ¼ entire length of enamel ﬁgure 2 ¼ absent 31. Amplitude of enamel folding 0 ¼ absent 1 ¼ high 2 ¼ low 32. Spacing between enamel folds 0 ¼ absent 1 ¼ tight 2 ¼ loose 33. Crenated versus smooth enamel 0 ¼ Smooth 1 ¼ Crenated *May be taphonomic Cranial characters 34. Parietal/Occipital crest (¼nuchal ridge) 0 ¼ pronounced ridge 1 ¼ ridge 2 ¼ smooth 35. Shape of nares opening 0 ¼ ‘‘dumbell’’ shaped 1 ¼ turned down at lateral edges 2 ¼ rounded and turned up at lateral edges *May be related to sexual dimorphism (frontal view) 36. Borders of nares opening 0 ¼ sharp and pronounced 1 ¼ smooth and rounded 37. Center of nuchal ridge 0 ¼ smooth and even 1 ¼ heart-shaped 2 ¼ concave (frontal view) 38. Position of orbits relative to tooth row 0 ¼ anterior to tooth row 1 ¼ even with beginning of toothrow 2 ¼ posterior to beginning of tooth row 39. Slope of forehead and premaxillaries 0 ¼ premaxillaries steeper than forehead 1 ¼ in same plane 2 ¼ forehead steeper than premaxillaries (lateral view) 40. Temporal line 0 ¼ smooth 1 ¼ line 2 ¼ ridge 41. Parietal depression 0 ¼ absent 1 ¼ muscle marking 2 ¼ furrow 81 82 TODD TABLE 3. Cranial, dental, and mandible characters used in the cladistic analysis (continued) Dental characters 42. Occipitals 0 ¼ bulbous 1 ¼ ﬂat 43. Slope of occipitals from condyles 0 ¼ anterior 1 ¼ vertical 2 ¼ posterior (lateral view) 44. Position of supraoccipital relative to squamosal 0 ¼ directly superior 1 ¼ lateral 2 ¼ medial (posterior view) 45. Alveolar border of premaxillaries 0 ¼ even 1 ¼ slopes down laterally (inferior view) 46. Premaxillaries 0 ¼ parallel 1 ¼ ﬂared 2 ¼ straight-sided but diverging (inferior view) *May be related to sexual dimorphism 47. Shape of occipital condyles 0 ¼ round or square 1 ¼ triangular, elongated triangle 2 ¼ ‘‘bean’’ shaped 48. Condylar fossa 0 ¼ ﬂat and wide 1 ¼ ﬂat and narrow 2 ¼ deep and wide 3 ¼ deep and narrow 49. Condylar facet 0 ¼ even with fossa 1 ¼ slopes posteriorly from fossa 2 ¼ slopes anteriorly from fossa 50. Basio-occipital 0 ¼ plate-like, with pronounced edges 1 ¼ smooth, completely fused 51. Basio-occipital and vomer 0 ¼ meet 1 ¼ separated 52. Position of exoccipital relative to condyles 0 ¼ lateral 1 ¼ anterior (posterior view) 53. Forehead 0 ¼ rounded 1 ¼ ﬂat 2 ¼ concave (lateral view) 54. Tusk sheaths 0 ¼ rotated anteriorly 1 ¼ even 2 ¼ rotated posteriorly (inferior view) 55. Ventral depression of palate 0 ¼ no 1 ¼ yes 56. Position of occipital condyles relative to tooth row 0 ¼ posterior 1 ¼ in line with end of tooth row PHYLOGENETIC ANALYSIS OF THE ELEPHANTIDAE TABLE 3. Cranial, dental, and mandible characters used in the cladistic analysis (continued) Dental characters 57. Opening of external nares 0 ¼ above orbit 1 ¼ even with orbit 2 ¼ below orbit (lateral view) 58. Anterior portion of zygomatic 0 ¼ projecting anteriorly 1 ¼ receding 59. Premaxillaries 0 ¼ Directed out and forward 1 ¼ Directed out and downward (lateral view) 60. Height of occipital condyles 0 ¼ low 1 ¼ elevated 61. Frontal bones 0 ¼ elongated 1 ¼ shortened 62. Skull shape 0 ¼ rounded 1 ¼ compressed parallel to facial plane (lateral view) 63. Palate keel 0 ¼ absent 1 ¼ present 64. Nuchal fossa 0 ¼ deep 1 ¼ shallow 65. Occipital bosses 0 ¼ in facial plane 1 ¼ overhang forehead (lateral view) Mandible characters 66. Mandibular condyle shape 0 ¼ long anterio-posteriorly 1 ¼ oval 2 ¼ rectangular 67. Condyle surface 0 ¼ slopes medially 1 ¼ even 68. Ascending rami 0 ¼ diverging 1 ¼ curve in 2 ¼ parallel 69. Mandibular symphysis 0 ¼ directed forward 1 ¼ directed down 70. Length of mandibular symphysis 0 ¼ long 1 ¼ intermediate 2 ¼ short *Relative character 71. Shape of symphyseal trough 0 ¼ horseshoe shaped 1 ¼ U-shaped 2 ¼ V-shaped 72. Mandibular corpus 0 ¼ swollen 1 ¼ gracile (posterior view) (frontal view) 83 84 TODD TABLE 3. Cranial, dental, and mandible characters used in the cladistic analysis (continued) Dental characters 73. Position of coronoid process relative to maximum length of corpus 0 ¼ posterior 1 ¼ half way 2 ¼ anterior (lateral view) 74. Lateral side of ascending ramus 0 ¼ concave 1 ¼ ﬂat 75. Angle of ascending ramus relative to corpus 0 ¼ 90 angle 1 ¼ acute angle (lateral view) 76. Height of ascending ramus relative to maximum length of corpus 0 ¼ ramus height < corpus length 1 ¼ ramus height ¼ corpus length 2 ¼ ramus height > corpus length (lateral view) 77. Lower incisors 0 ¼ present 1 ¼ germ cavity 2 ¼ absent Fig. 3. Ordered analysis of dental characters with successive weighting produced one tree. The genera are color coded. African Elephas is in blue, and the Eurasian Elephas in light blue. Loxodonta is paraphyletic, Elephas is polyphyletic. Stegodon kaisensis is the outgroup. DISCUSSION Homoplasy is a persistent problem in this cladistic analysis. All three lineages are undergoing similar trends in character evolution, but at different rates and times. As a result, each character appears on the tree several times, resulting in low CI indices. In two clades from an analysis of subspecies and species (Todd, 2006), the dental similarities are clearly seen (Fig. 5,6). Some of these similarities have phylogenetic signiﬁcance, (Elephas iolensis and Elephas hysudricus), while others illus- Fig. 4. Unordered analysis of dental characters with successive weighting produced two trees. The only difference between the two trees is the position of S. orbus and P. gomphotheroides. The genera are color coded. African Elephas is in blue and the Eurasian Elephas in light blue. In this cladogram, Loxodonta is polyphyletic, and Elephas is paraphyletic. trate the unique problems of parallel evolution, and the difﬁculty in sorting out homoplasy resulting from convergence (Loxodonta atlantica and Elephas recki recki). This creates a problem using parsimony, but it is possible to make conclusions about phylogenetic relationships if this complication due to parallel evolution is kept in consideration, and a new phylogeny is presented in Fig. 7. Loxodonta is paraphyletic in both analyses of cranial and dental characters. Elephas is polyphyletic in the ordered analysis but paraphyletic in the unordered analysis due to the inclusion of Mammuthus primigenius with Fig. 5. In a previous cladistic analysis of subspecies within the elephantidae (Todd, 1997), the problem of homoplasy is illustrated by the phenotypic similarities in several molar characters among African and European Elephas and Loxodonta. Fig. 6. In a previous cladistic analysis of subspecies within the elephantidae (Todd, 1997), all ﬁve subspecies of Elephas recki fail to group together, and some of these subspecies share similarities with Loxodonta and Eurasian Elephas. 86 TODD Fig. 7. New phylogeny of the Elephantidae based on the cladistic analysis. Loxodonta adaurora and Mammuthus are consolidated into one lineage leading from Stegotetrabelodon and Elephas and the main lineages of Loxodonta evolves from Primelephas. Age range and locality data obtained from: Asfaw et al. (1991), Andrews et al. (1981), Aouadi (2001), Beden (1979, 1981, 1987), Behrensmeyer et al. (1995, 1997, 2002), Boaz et al. (1992), Brown (1985), Caloi et al. (1996), Cerling et al. (1999), Cooke (1993), Cooke and Coryndon (1970), Coppens (1972), Coppens et al. (1978), Court (1995), Debruyne et al. (2003), deBonis et al. (1988), Deino and Hill (2002), Gaziry (1987), Gheerbrant et al. (1996, 1998, 2002), Harrison and Baker (1997), Hill (1995), Hill et al. (2002), Jacobs et al. (1999), Kalb et al. (1982), Kalb and Mebrate (1993), Kingston and Harrison (2003), Kingston et al. (2002), Klein (1973-74), Labe and Guerin (2005), Leakey et al. (1995, 1996), Lister (1996), Lister et al. (2005), Maglio (1970a, 1970b, 1972, 1973), Morgan et al. (1994), Nanda (2002), Osborn (1931, 1936, 1942), Pickford (1988), Plummer and Potts (1989), Poulakakis et al. (2002), Raynal et al. (1990), Rogaev et al. (2006), Sanders (1990), Sanders et al. (2002), Shipman et al. (1981), Shoshani (1996), Shoshani and Tassy (1996, 2005), Smart (1976), Tassy (1986, 2003), Tassy and Debryune (2001), Tassy et al. (2003), Todd (1999, 2005, 2006), Todd and Roth (1996), White et al. (1984), Wolde Gabriel et al. (1994). the Eurasian Elephas species. In the analysis of dental characters only, Loxodonta is paraphyletic in the ordered analysis but polyphyletic in the unordered analysis. Mammuthus is also paraphyletic in both analyses. There are many other species of Mammuthus that could be included in this analysis, but these are middle to late Pleistocene forms that are highly derived. The three species included here are the older, more ancestral species. Both Mammuthus meridionalis and Mammuthus armeniacus remain together as a clade, but do not group with Mammuthus subplanifrons. Based on the results of previous metric analysis of the family elephantidae, M. sub- planifrons is inseparable from Loxodonta adaurora, an early loxodont species in Africa (Todd, 1997). Considering these results, and that M. subplanifrons consistently groups with L. adaurora as a basal member of the Elephantidae in the cladistic analysis, it is highly likely that these two species are the same species. This partially solves the homoplastic problem of Loxodonta, at least in the unordered analysis. There are certain features of the skull of L. adaurora which are similar to later mammoths including massive, ﬂaring premaxillaries, twisted tusks (although straight), and a relatively ﬂat frontal. This suggests that L. adaurora does not PHYLOGENETIC ANALYSIS OF THE ELEPHANTIDAE 87 Fig. 8. Beden’s (1979) phylogeny included Stegotetrabelodon as the potential ancestor for the family. He also proposed several migrations of Elephas out of Africa into Eurasia. He also separated L. adaurora from the main Loxodonta lineage. He also uses Elephas and Paleoloxodon as subgenera for the African Elephas lineage. belong in the Loxodonta lineage, and may, combined with M. subplanifrons, represent the primitive mammoth condition. The grouping of Stegotetrabelodon with L. adaurora supports Beden’s (1979) phylogeny (Fig. 8). Both Maglio and Beden proposed Primelephas as the ancestor of Elephas and Mammuthus (and Maglio included Loxodonta as a descendant) and the position of Primelephas gomphotheroides as ancestral is supported in the cladistic analysis. However, the cladistic analysis, and previous metric analysis (Todd, 1997) suggests a closer relationship between Stegotetrabelodon and L. adaurora. Combined with the conclusion stated previously that M. subplanifrons and L. adaurora are the same species; this suggests that Stegotetrabelodon is ancestral to Loxodonta and Mammuthus. Primelephas is ancestral to Elephas only (Fig. 8). Both Maglio and Beden divided Elephas recki into smaller taxonomic units, Stages 1–4 by Maglio, Elephas recki brumpti, E. r. shungurensis, E. r. atavus, E. r. ileretensis, and E. r. recki by Beden. There is still much variation even within these groups, and E. recki as proposed is not a valid species (Todd, 2005). There are specimens that belong to Loxodonta and Mammuthus, as well as Elephas and the Paleoloxodon group that had been previously attributed to E. recki. Originally, a subgenus of Elephas, Paleoloxodon is resurrected in this new phylogeny, and includes specimens previously attributed to E. recki from 2.5 to 4 ma in Africa. Subspecies designations for E. recki are no longer considered valid (Fig. 7). In Maglio’s (1973) phylogeny, he includes one migration out of Africa for Elephas, that subsequently underwent an adaptive radiation in Eurasia (Fig. 9). Beden (1979) proposed two migrations of Elephas out of Africa; an earlier wave that evolved into Elephas (Elephas), and a second, younger wave that he designates Elephas (Paleoloxodon) due to similarities of these species to the African Elephas recki lineage. In this analysis, the Eurasian Elephas species, Elephas namadicus and Elephas antiquus, group together with the extant Elephas 88 TODD Fig. 9. In Maglio’s (1973) phylogeny, he includes Primelephas as the ancestor to the Elephantidae, and only one migration event of Elephas out Africa into Eurasia, where the lineage subsequently underwent an adaptive radiation. maximus and with Elephas meletensis consistently in both ordered and unordered cladograms. E. recki and Elephas iolensis (African species) group consistently with Elephas hysudricus (Eurasian) and Elephas mnaidriensis (Mediterranean dwarf). The cladistic analysis presented here supports Beden’s phylogeny of two separate migrations out of Africa for Elephas, with potentially two separate dwarﬁng events in the Mediterranean groups, although the allometric issues involved with reduction in body size in elephants is potentially generating homoplastic noise and this needs further study. Maglio (1973) and others ﬁrmly place E. hysudricus as the ancestor to E. maximus. In this analysis, E. maximus does not form a clade with E. hysudricus and E. iolensis. However, previous metric data supports the relationship, and it is retained here for now (Todd, 1997). The wide range of metric variation in dentition in the African Elephas group, as well as the Eurasian species complicates the situation, and much further work is needed. The retention of a lozenge-like shape to the enamel ﬁgure in E. recki, E. antiquus, and E. namadicus, as well as with the dwarfed Mediterranean species, suggests an evolutionary relationship, as do various cranial similarities, such as large parietal bosses that overhang the forehead. There are recent data supporting the inclusion of some of the Mediterranean dwarfs in Mammuthus (Poulakakis et al., 2002), and this is an interesting possibility. Elephas hysudricus, Elephas planifrons, Elephas maximus, and other Eurasian species have parallel-sided enamel ﬁgures, much thinner enamel and more lamellae. Thus, there may be support here for two separate genera within the Elephas group, an Elephas group that migrates out of Africa 3.7 ma, and potentially back to Africa with Elephas iolensis, and a Paleoloxodon group that leaves Africa 2.5 ma (Fig. 7). This cladistic study relies heavily on dentition, which appears to be highly variable in fossil species and lineages, and again, more analysis is needed on cranial characters which suggest speciﬁc evolutionary PHYLOGENETIC ANALYSIS OF THE ELEPHANTIDAE relationships between African and Eurasian species. In addition, examination of postcranial elements potentially adds further data for comparisons. This is the ﬁrst cladistic analysis to focus speciﬁcally on the Elephantidae as a whole, and the ﬁrst new phylogenetic proposal in many years. Much comparative study remains to be done, as well as analysis of metric variation in fossil and modern elephants in order to further elucidate the complicated evolutionary relationships within this family. ACKNOWLEDGMENTS This study would not have been possible without the permission of the Directors and Curators at the following museums: American Museum of Natural History, National Museum of Natural History, National Museums of Kenya, Tanzanian Museum, Musée Nationale d’Histoire Naturelle, British Museum of Natural History, and the Royal Ontario Museum. In addition, the author thanks many who helped with comments and information along the way, particularly P. Tassy, W. Sanders, M. Leakey, T. Harrison, J. Kalb, J. Kingston, A. Lister, L. Agenbroad, E. Sargis, T. Plummer, R. Potts, K. Behresmeyer, A. Brooks and D. Lipscomb. LITERATURE CITED Asfaw B, Beyene Y, Semaw S, Suwa G, White TD, WoldeGabriel, G. 1991. Fejej: a new paleoanthropological research area in Ethiopia. J Hum Evol 21:137–143. Andrews PJ, Meyer GE, Pilbeam DR, Van Couvering JA, Harris J. 1981. The Miocene fossil beds of Maboko Island, Kenya: geology, age, taphonomy, and paleoecology. J Hum Evol 10:35–48. Aouadi N. 2001. 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