Phylogenetic relationships and limb loss in sub-Saharan African scincine lizards (Squamata: Scincidae)

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Abstract

Skinks are the largest family of lizards and are found worldwide in a diversity of habitats. One of the larger and more poorly studied groups of skinks includes members of the subfamily Scincinae distributed in sub-Saharan Africa. Sub-Saharan African scincines are one of the many groups of lizards that show limb reduction and loss, and the genus Scelotes offers an excellent opportunity to look at limb loss in a phylogenetic context. Phylogenetic relationships were reconstructed for a total of 52 taxa representing all subfamilies of skinks as well as other Autarchoglossan families using sequence from six gene regions including; 12S, 16S, and cytochrome b (mitochondrial), as well as α-Enolase, 18S, and C-mos (nuclear). The family Scincidae is recovered as monophyletic and is the sister taxon to a (Cordylidae + Xantusiidae) clade. Within skinks the subfamily Acontinae is monophyletic and sister group to all remaining skinks. There is no support for the monophyly of the subfamilies Lygosominae and Scincinae, but sub-Saharan African scincines + Feylinia form a well supported monophyletic group. The monophyly of Scelotes is confirmed, and support is found for two geographic groups within the genus. Reconstructions of ancestral states for limb and digital characters show limited support for the reversal or gain of both digits and limbs, but conservative interpretation of the results suggest that limb loss is common, occurring multiple times throughout evolutionary history, and is most likely not reversible.

Introduction

With more than 1300 species, skinks comprise the largest family (Scincidae) of lizards, and include >25% of the world’s lizard diversity (Bauer, 1998). Greer (1970b) defined four subfamilies within skinks that are still widely used today. The Acontinae (18 spp.) and Feylininae (4 spp.) are small groups of completely limbless skinks restricted to Africa. The Lygosominae is the largest and most speciose subfamily and is distributed worldwide, but with the majority of its diversity in Australia and Asia. Like the two small subfamilies, the monophyly of the Lygosominae has generally been accepted on the basis of derived morphological features (Greer, 1970b, Greer, 1986; Griffith et al., 2000; but see Hutchinson, 1981). The Scincinae is also a large subfamily distributed throughout the Americas and Asia, but with its center of diversity in Africa. Greer (1970b) postulated that scincines were primitive, originated in Africa, and independently gave rise to the other three subfamilies. The recognized paraphyly of the Scincinae has long been an impediment to the resolution of higher order skink relationships. Recently, Greer and Shea (2000) described the shared occurrence of a derived head scale pattern (the “chalcidine” condition) characterizing all non-lygosomine skinks except Eumeces, Scincus, and Scincopus and Griffith et al. (2000) have proposed a fifth subfamily, the Eumecinae, in an attempt to identify monophyletic subgroups within the Scincinae sensu Greer (1970b).

One of the most poorly studied groups of scincines consists of the seven genera occurring in sub-Saharan Africa. One of these, Chalcides, is chiefly Mediterranean in its distribution, and has been the subject of relatively intensive systematic study (Brown and Pestano, 1998; Caputo, 1993; Caputo et al., 1999). Among the remaining taxa, four genera: Typhlacontias, Sepsina, Proscelotes, and Scelotes, occur chiefly in southern Africa (south of the Kunene and Zambezi Rivers), while two genera: Scolecoseps and Melanoseps are restricted to tropical east and central Africa. The affinities of some of these forms, as well as the taxa now allocated to the Acontinae and Feylininae, were considered by de Witte and Laurent (1943). They grouped Sepsina with the acontines and Scelotes, Scolecoseps, Melanoseps, and Typhlacontias with the feylinines, while regarding Proscelotes as ancestral to both lineages. Greer, 1970a, Greer, 1970b accepted some of these relationships, but considered Sepsina and Proscelotes as closely related and regarded acontines, feylinines, and scincines as phylogenetically distinct from one another.

Among the southern African scincines the genus Scelotes, with 21 species, is by far the most diverse group. The genus was originally described by Fitzinger (1826), and has been investigated by Hewitt, 1921, Hewitt, 1927, Hewitt, 1929, Barbour and Loveridge (1928), de Witte and Laurent (1943), and FitzSimons (1943). The last of these reviews synonymized Sepsina with Scelotes, but confirmed the placement of Malagasy forms in a separate genus, Amphiglossus. Greer (1970a) reduced the total number of Scelotes species to 14, revalidating Sepsina and including the East African species uluguruensis in Scelotes. Broadley’s recent monograph (1994) brought the total number of species to 21, and postulated certain interspecific relationships based on limb, eyelid, and scale characters. To date there have been no molecular data presented nor formal cladistic analyses conducted for Scelotes or for sub-Saharan African scincines as a whole (but see Brown and Pestano, 1998; Caputo et al., 1999; Haacke, 1997 for analyses of Chalcides and Typhlacontias, respectively). Although an explicit phylogeny of Scelotes and its relatives is desirable in its own right, it also provides the basis for the investigation of the evolution of limb reduction, which characterizes many of the African scincines and numerous other clades of lizards (Camp, 1923; Gans, 1975; Lande, 1977; Presch, 1975; Wiens and Slingluff, 2001).

Limb loss or reduction is an interesting phenomenon seen in many clades of squamates including snakes, amphisbaenids, and dibamid, teiid, gymnopthalmid, pygopodid, anguid, cordylid, and scincid lizards. The occurrence of limb loss in multiple squamate lineages leads to questions concerning the evolutionary pattern or stages of limb loss, and the developmental mechanisms and pathways involved (Wiens and Slingluff, 2001). Species within each of the currently recognized subfamilies of skinks, except the Eumecinae, demonstrate complete external limb loss, and it is postulated that limb reduction in some form has occurred more than 30 times within skinks (Bauer, 1998; Greer, 1991). The most speciose lineage to exhibit limb reduction, and that with the finest gradations in loss, is the Australian lygosomine genus Lerista (Greer, 1987, Greer, 1990, Greer, 1991; Hauser, 1996; Kendrick, 1991). Among scincines the greatest variation in limb expression occurs in the southern African genus Scelotes, which exhibits a morphocline from fully functional pentadactyl limbs to complete limblessness, with many species showing seemingly transitional stages in reduction of digits and limbs. Due to this variation, Scelotes offers an exceptional system in which to study limb loss in a phylogenetic context. In particular, Scelotes may be used to test the hypothesis that limb and digital loss is irreversible (Dollo’s Law; Gould, 1970).

The purposes of this paper are: (1) test the monophyly of sub-Saharan African scincines, (2) test the monophyly of Scelotes, (3) establish a preliminary estimate of phylogeny for sub-Saharan African scincines (specifically Scelotes) based on molecular data, and (4) evaluate limb and digital loss in a phylogenetic context within this group.

Section snippets

Sampling

Taxon sampling focused on sub-Saharan African scincines (5/7 genera), with an emphasis on southern African forms (4/4 genera) and more specifically on the genus Scelotes (9/21 spp.). In total, 36 taxa representing all four subfamilies of skinks (sensu Greer, 1970b) were sequenced, including Scincinae (7 genera, 18 spp.), Acontinae (2 genera, 3 spp.), Feylininae (1 genus, 1 sp.), and Lygosominae (8 genera, 12 spp.; see Table 1). In order to test the monophyly and placement of Scincidae,

Molecular data

The molecular data collected include approximately 5000 bases across six gene regions for 52 taxa (see Table 1). Uncorrected pairwise sequence divergence for each gene across all taxa, within skinks, within sub-Saharan African scincines, and within Scelotes are shown in Table 4. These divergence profiles reflect great variation in the rates of evolution among the markers, and suggest their phylogenetic utility at different taxonomic levels.

Optimization alignment

Tree lengths for all optimization alignment (OA)

Sister group to skinks

While the monophyly of Scincidae is confirmed in all analyses, the sister group to skinks does vary in sensitivity analyses (see Table 6). Past studies within Scincomorpha have found strong support for a sister group relationship between skinks and cordylids (Scincoidea) (Estes et al., 1988; Odierna et al., 2002; Schwenk, 1988; Vicario et al., 2003), but the placement of Xantusiidae has been problematic (Estes, 1983; Estes et al., 1988; Evans and Chure, 1998; Lang, 1991; Lee, 1998; Macey et

Conclusions

This study is the first to use molecular data to investigate relationships among sub-Saharan African scincines, and is the largest sampling of genes ever generated for skinks. Within sub-Saharan African scincines Scelotes, Proscelotes, and Sepsina form one clade, while Typhlacontias, Melanoseps, and Feylinia compose a second, primarily limbless clade. These results and the monophyly of sub-Saharan African scincines provide the necessary outgroup information and will be the foundation for all

Acknowledgements

Special thanks go to J. Vindum and R.C. Drewes (California Academy of Sciences), J. Gauthier (Yale Peabody Museum), J.D. Harris (Unidade de Genética Animal e Conservação), K. Pellegrino and M.T. Rodrigues (Universidade de São Paulo), R. Bezy (Los Angeles County Museum), C. White (Brigham Young University), A. Schmitz (Zoologisches Forschungsinstitut und Museum Alexander Koenig), M. Griffin (Ministry of Environment and Tourism, Republic of Namibia), N. Kley (University of Massachusetts), A.

References (101)

  • M.S.Y. Lee

    Convergent evolution and character correlation in burrowing reptiles: towards a resolution of squamate relationships

    Biol. J. Linn. Soc.

    (1998)
  • K.C. Nixon et al.

    On simultaneous analysis

    Cladistics

    (1996)
  • G. Odierna et al.

    A phylogenetic analysis of Cordyliformes (Reptilia: Squamata): comparison of molecular and karyological data

    Mol. Phylogenet. Evol.

    (2002)
  • K.C.M. Pellegrino et al.

    A molecular perspective on the evolution of microteiid lizards (Squamata, Gymnophthalmidae), and a new classification for the family

    Biol. J. Linn. Soc.

    (2001)
  • A. Phillips et al.

    Multiple sequence alignment in phylogenetic analysis

    Mol. Phylogenet. Evol.

    (2000)
  • K.M. Saint et al.

    C-mos, a nuclear marker useful for Squamate phylogenetic analysis

    Mol. Phylogenet. Evol.

    (1998)
  • S. Vicario et al.

    Xantusiid “night” lizards: a puzzling phylogenetic problem revisited using likelihood-based Bayesian methods on mtDNA sequences

    Mol. Phylogenet. Evol.

    (2003)
  • W.C. Wheeler

    Fixed character states and the optimization of molecular sequence data

    Cladistics

    (1999)
  • W.C. Wheeler et al.

    The phylogeny of the extant hexapod orders

    Cladistics

    (2001)
  • R.H. Baker et al.

    Multiple sources of character information and the phylogeny of hawaiian drosophilids

    Syst. Biol.

    (1997)
  • T. Barbour et al.

    A comparative study of the herperological faunae of the Uluguru and Usambara Mountains, Tanganyika Territory with descriptions of new species

    Mem. Mus. Comp. Zool. Harvard Coll.

    (1928)
  • A.M. Bauer

    Lizards

  • G.A. Boulenger

    Synopsis of the families of existing Lacertilia

    Annu. Mag. Nat. Hist.

    (1884)
  • W.R. Branch et al.

    Herpetofauna of the Little Karoo, Western Cape, South Africa with notes on life history and taxonomy

    Herpetol. Nat. Hist.

    (1995)
  • D.G. Broadley

    The genus Scelotes Fitzinger (Reptilia: Scincidae) in Mozambique, Swaziland and Natal, South Africa

    Ann. Nat. Mus.

    (1994)
  • R.P. Brown et al.

    Phylogeography of skinks (Chalcides) in the Canary Islands inferred from mitochondrial DNA sequences

    Mol. Ecol.

    (1998)
  • C.L. Camp

    Classification of the lizards

    Bull. Am. Mus. Nat. Hist.

    (1923)
  • V. Caputo

    Taxonomy and evolution of the Chalcides chalcides complex (Reptilia: Scincidae) with description of two new species

    Boll. Mus. Reg. Sci. Nat. Torino

    (1993)
  • V. Caputo et al.

    A molecular taxonomy of some Mediterranean scincid lizards, genus Chalcides Laurenti 1768 (Reptilia: Scincidae)

    Russ. J. Herpet.

    (1999)
  • P.T. Chippindale et al.

    Weighting, partitioning and combining characters in phylogenetic analysis

    Syst. Biol.

    (1994)
  • E.D. Cope

    A contribution to the herpetology of Mexico. I. The collection of the Comision Cientifica

    Proc. Am. Herp. J. Soc.

    (1885)
  • C.W. Cunningham

    Some limitations of ancestral character state reconstruction when testing evolutionary hypotheses

    Syst. Biol.

    (1999)
  • G.F. de Witte et al.

    Contribution à la systématique des formes dégradées de la famille des Scincidae apparentées au genre Scelotes Fitzinger

    Mém. Mus. R. Hist. Nat. Belg

    (1943)
  • J.J. Doyle

    Gene trees and species trees: molecular systematics as one character taxonomy

    Syst. Bot.

    (1992)
  • J.J. Doyle

    Trees within trees: genes and species, molecules and morphology

    Syst. Biol.

    (1997)
  • D.J. Eernisse et al.

    Taxonomic congruence versus total evidence, and amniote phylogeny inferred from fossils, molecules, and morphology

    Mol. Biol. Evol.

    (1993)
  • R.G. Estes

    Sauria Terrestria, Amphisbaenia

    (1983)
  • R.G. Estes et al.

    Phylogenetic relationships within Squamata

  • S.E. Evans et al.

    Paramacellodid lizard skulls from the Jurassic Morrison Formation at Dinosaur National Monument

    Utah J. Vert. Paleo.

    (1998)
  • FitzSimons, V.F., 1943. The Lizards of South Africa. Mem. Transvaal Mus. 1, 24 pls., map,...
  • V.L. Friesen et al.

    Intron variation in marbled murrelets detected using analyses of single-stranded conformational polymorphisms

    Mol. Ecol.

    (1997)
  • D. Frost et al.

    A molecular perspective on the phylogeny of the girdled lizards (Cordylidae, Squamata)

    Am. Mus. Nov.

    (2001)
  • P.C. Frumhoff et al.

    Using phylogenies to test hypotheses of adaptation: a critique of some proposals

    Evolution

    (1994)
  • C. Gans

    Tetrapod limblesness: evolution and functional corollaries

    Am. Zool.

    (1975)
  • Gladstein, D., Wheeler, W.C., 1999–2002. POY: Phylogeney Reconstruction via direct optimization of DNA data, 2.0 and...
  • J.S. Gould

    Dollo on Dollo’s: irreversibility and the status of evolutionary laws

    J. Hist. Biol.

    (1970)
  • A. Graybeal

    Evaluating the phylogenetic utility of genes: a search for genes informative about deep divergences among vertebrates

    Syst. Biol.

    (1994)
  • A.E. Greer

    The systematics and evolution of the subsaharan Africa, Seychelles, and Mauritius scincine scincid lizards

    Bull. Mus. Comp. Zool.

    (1970)
  • A.E. Greer

    A subfamilial classification of scincid lizards

    Bull. Mus. Comp. Zool.

    (1970)
  • A.E. Greer

    A phylogenetic subdivision of Australian skinks

    Rec. Aust. Mus.

    (1979)
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