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Phylogenetic Relationships and Evolutionary Patterns Based on Immunological Data

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Phylogenetic Relationships and Evolutionary Patterns Based on Immunological Data <oological journal of the Linnean Society (1994), 110: 103-140. With 3 figures The colubrid radiation in Africa (Serpentes: Colubridae): phylogenetic relationships and evolutionary patterns based on immunological data JOHN E. CADLE Museum of Comparative <oologv, Harvard University, Cambridge, MA 02138, U.S.A. Received December 1992, revised and accepted May 1993 Phylogenetic relationships among genera of African colubrids were evaluated using estimates of divergence among serum albumins compared by microcomplement fixation. Representatives of about half of the extant genera of African colubrids, as well as the Elapidae, Atractaspis and the Madagascan colubrid Leioheterodon, were analysed. The tree of best fit to the data has an unresolved basal polychotomy comprising at least five lineages of colubrids, as well as Elapidae and Atractaspis; thus, colubrids were not demonstrably monophyletic with these data. Two cosmopolitan clades, colubrines and natricines, are represented in Africa by series of closely related genera, but divergence among other genera is relatively great. Rate tests show that this is apparently not due to higher rates of albumin evolution in these, relative to other colubrids. Among the other associations supported by the immunological data are: (I) Psammophis-(Rhamphiophis-Dipsina)-Malpolon- Psarnmophylax; (2) Ambhodipsas-Macrelaps; (3) (Lycodonomorphus-Lamprophis)-Meheha; and (4) Colubrinae-Natricinae. Grayia is questionably associated with the colubrine-natricine lineage. Prosymna and Lycodon are clearly members of the colubrine clade, and Amplorhinus possibly associates with Leioheferodon. Gonionotophis, Duberria, Lycophidion and Pseudaspis show no strong association with any other genera, and represent other basal or near-basal clades within the colubridlelapid radiation. The immunological data do not support a clade comprising the Elapidae, Atractaspic and some ‘aparallactines’ relative to Viperidae and other colubrids. The basal colubrid-elapid-Afractaspis divergence occurred more than 30 Myr ago, and the fossil record of colubrids in Africa greatly underestimates both the age and clade diversity of this group. In contrast to the pattern of radiation in the neotropics, where most colubrids belong to one of three major clades, in Africa only the colubrine lineage comprises a substantial portion of the extant generic diversity; most other genera stem from relatively ancient cladogenetic events and have few living representatives. ADDITIONAL KEY WORDS:-Africa - snakes - systematics - biogeography - phylogeny molecular systematics - albumin. CONTENTS Introduction . 104 Bogert’s arrangement of African colubrids and the scope of the present work. 105 This paper is dedicated to the memory of Charles M. Bogert (1908-1992), who not only pioneered the modern study of African colubrid systematics but also showed us the way in many other areas of reptile biology. 103 0024-4082/94/002 103 + 38 $08.00/0 0 1994 The Linnean Society of London 104 J. E. CADLE Materials and methods . 107 Antigens and antisera . 107 Basic taxa, outgroups, and phylogenetic trees . 107 Results . 111 Reciprocal comparisons and phylogenetic trees . 111 Rate tests for albumin evolution in African colubrids . 1 I3 Unidirectional comparisons (Bogert’s Groups 1, 2, 5-7, 12, 16, 17) . 114 Lycodon and the status of the Lycodontinae . 118 Psammophis-Rhamphiophis clade (Bogert’s Group 16) . 119 Comments on McDowell’s (1986) Homoroselaps Group (Bogert’s Groups 7 and 17) . 121 Problems in colubrid phylogeny . 123 Discussion . 124 Other immunological data bearing on higher relationships among colubrids . 124 Bogert’s arrangement of African colubrids in retrospect . 127 The fossil record of snakes in Africa and the age of its colubrid lineages . 128 Biogeographic considerations . 130 A comparison of African and Neotropical colubrid radiations . 132 A note on nomenclature of higher taxa within colubrids . 133 Acknowledgements . 136 References . 137 .4ppendix . 140 INTRODUCTION The central importance of Africa for understanding the evolutionary and biogeographic history of Gondwanan and Laurasian taxa has been widely acknowledged (Maglio & Cooke, 1978; Storch, 1990, 1992; Gheerbrant, 1990; Rage, 1988a; Ciochon & Chiarelli, 1980). Recent fossil discoveries from Africa and elsewhere have sharply focused attention on our poor understanding of the relationship between Africa and its early Tertiary neighbours. These discoveries provide new insights into the composition of early African faunas (e.g. marsupials in the Eocene and Oligocene [Crochet, 1984, 1986; Bown & Simons, 19841; tarsiiform and possible anthropoid primates from the early Tertiary [Simons & Bown, 1985; Godinot & Mahboubi, 1992; Simons, 19921, and faunal exchanges with other regions (Bernor, 1983; Bernor et al., 1987; Rage, 1988a). These discoveries and improvements in understanding the phylogenetic relationships of Africa’s many endemic groups, have resulted in more complete understanding of faunal evolution on that continent and its bearing on faunal evolution on other continents throughout the Cenozoic (Maglio & Cooke, 1978; Bernor et al., 1987; Storch, 1992). Long-standing hypotheses about the biogeographic histories of some groups have been questioned or revised to reflect these findings (Martin, 1985; Benton, 1985; Bernor et al., 1987; Janis, 1988; Culotta, 1992; Gheerbrant, 1990; Ciochon & Chiarelli, 1980). Nevertheless, much of the early history of Africa remains shrouded in mystery as a result of the paucity of Tertiary terrestrial fossil-bearing deposits in Africa (Savage, 1967; Cooke, 1978; Winkler, 1992). Hence, studies of the phylogenetic relationships of the extant fauna continue to play major roles in formulating hypotheses for the evolutionary history of the African fauna (Luckett & Hartenberger, 1985). This is especially true for groups such as snakes, which have a very poor fossil record in Africa, as in all tropical regions (Rage, 1973; Meylan, 1987; Cadle, 1987). Of special concern for understanding the Tertiary history of Africa are relationships between some African and South American lineages. The most PHYLOGENY OF AFRICAN COLUBRIDS 105 extensively-studied examples are the endemic platyrrhine primates of the Neotropics, and hystricognath rodents, found in both Africa and South America (both groups reviewed in Ciochon & Chiarelli, 1980; see also Luckett & Hartenberger, 1985). The potential relevance of African lineages to understanding the evolutionary history of several clades of endemic neotropical snakes of the family Colubridae was recognized early in a broad-scale phylogenetic study using estimates of albumin divergence measured immunologically (Cadle, 1984a-c, 1985, 1988). An initial series of molecular comparisons revealed, however, that the situation in Africa was much more complicated than that in the neotropics, and exploration of African-Neotropical relationships was postponed until additional data concerning the phylogenetic structure of the colubrid radiation in Africa could be obtained. This report is a first exposition of the African situation. My goals in this paper are (1) to present a hypothesis of relationships among major lineages of African colubrids and other taxa of advanced (caenophidian) snakes (Elapidae, Atractaspis); (2) to evaluate the significance of the hypothesis for African colubrid systematics; (3) to use this hypothesis as a framework for evaluating some other hypotheses and scenarios for the evolution of advanced snakes; and (4) to examine some general characteristics of the radiation of African colubrids as compared to Neotropical radiations. The relevance of the phylogenetic hypotheses to aspects of the biogeographic and fossil history of African snakes is discussed, and some nomenclatural issues within Colubridae are addressed. BOGERT’S ARRANGEMENT OF AFRICAN COLUBRIDS AND THE SCOPE OF THE PRESENT WORK Perhaps the most influential modern work on the systematics of African colubrids is Bogert’s (1940) account of several collections made during the 1920s and 1930s. Bogert developed a comprehensive classification of African genera using features that Dunn (1928) found useful in assessing relationships among New World colubrids (vertebral hypapophyses, hemipenes and dentition), although the relative importance he ascribed to these features differed from Dunn’s. Bogert’s paper has formed the point of departure for much subsequent systematic work on African colubrids, and some of his groups have been given formal systematic status (see, for example, Bourgeois, 1968; Dowling, 1967, 1969; Dowling and Duellman, 1978). Using other sets of characters, particularly additional osteological and soft anatomical information, other workers have in some cases reached different conclusions from Bogert’s (1940) concerning the relationships of particular genera. Some of these differences are discussed below with reference to the immunological data. Bogert’s (1940) groups are summarized in Table 1 and are referred to in the text. However, discussion of immunological data on some of Bogert’s groups are deferred to future papers. These include Groups 8-10, 13-15 and 18, which collectively comprise a clade (along with many non-African representatives) relative to all other groups in Bogert’s scheme (Cadle, unpublished data). These are the Colubrinae, in the sense of Dowling et al. (1983) and McDowell (1987); the African members of these groups have been discussed by Rasmussen (1979, 1985). Likewise, Group 4 comprises genera usually referred to the Natricinae
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