Molecular systematics of the African snake family Lamprophiidae Fitzinger, 1843 (Serpentes: Elapoidea), with particular focus on the genera Lamprophis Fitzinger 1843 and Mehelya Csiki 1903

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Abstract

The snake family Lamprophiidae Fitzinger (Serpentes: Elapoidea) is a putatively Late Eocene radiation of nocturnal snakes endemic to the African continent. It incorporates many of the most characteristic and prolific of Africa’s non-venomous snake species, including the widespread type genus Lamprophis Fitzinger, 1843 (house snakes). We used approximately 2500 bases of mitochondrial and nuclear DNA sequence data from 28 (41%) of the approximately 68 recognised lamprophiid species in nine of the eleven genera to investigate phylogenetic structure in the family and to inform taxonomy at the generic level. Cytochrome b, ND4 and tRNA gene sequences (mitochondrial) and c-mos sequences (nuclear) were analysed using Maximum Likelihood, Bayesian Inference and Maximum Parsimony methods. The genus Mehelya Csiki, 1903 was paraphyletic with respect to Gonionotophis Boulenger, 1893. To address this, the concept of Gonionotophis is expanded to include all current Mehelya species. The genus Lamprophis emerged polyphyletic: the enigmatic Lamprophis swazicus was sister to Hormonotus modestus from West Africa, and not closely related to its nominal congeners. It is moved to a new monotypic genus (Inyoka gen. nov.). The remaining Lamprophis species occur in three early-diverging lineages. (1) Lamprophis virgatus and the widely distributed Lamprophis fuliginosus species complex (which also includes Lamprophis lineatus and Lamprophis olivaceus) formed a clade for which the generic name Boaedon Duméril, Bibron & Duméril, 1854 is resurrected. (2) The water snakes (Lycodonomorphus) were nested within Lamprophis (sensu lato), sister to Lamprophis inornatus. We transfer this species to the genus Lycodonomorphus Fitzinger, 1843. (3) We restrict Lamprophis (sensu strictissimo) to a small clade of four species endemic to southern Africa: the type species of Lamprophis Fitzinger, 1843 (Lamprophis aurora) plus Lamprophis fiskii, Lamprophis fuscus and Lamprophis guttatus.

Graphical abstract

The family Lamprophiidae is a putatively Late Eocene radiation of nocturnal, non-venomous African snakes. We use DNA sequence data to investigate phylogenetic structure within the family, and to inform taxonomy at the generic level. A new genus (Inyoka) is erected for the Swazi Rock Snake ’Lamprophis’ swazicus, the generic name Boaedon is resurrected for the ’Lamprophis’ fuliginosus species complex, ’Lamprophis’ inornatus is transferred to the genus Lycodonomorphus, and the genus Mehelya is placed in the synonymy of Gonionotophis.

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Research highlights

► A new genus (Inyoka) erected for the Swazi Rock Snake ‘Lamprophisswazicus. ► The generic name Boaedon resurrected for the ‘Lamprophisfuliginosus species complex. ► ‘Lamprophisinornatus transferred to the genus Lycodonomorphus. ► The genus Mehelya placed in the synonymy of Gonionotophis.

Introduction

There is a marked lack of consensus in contemporary literature regarding usage of the snake family name Lamprophiidae (Serpentes: Elapoidea) and its variants. Originating as the family Lamprophes Fitzinger, 1843, the name included in its disparate selection of taxa from Africa, Asia, the Americas and Australia, the genus Homalosoma containing the subgenus Lamprophis. Subsequently Bourgeois (1968) suggested that her ‘primitive’ grouping called Colubrinae africains (comprising Bothrophthalmus, Glypholycus [=Lycodonomorphus], Boaedon [=Lamprophis], Lamprophis, Natriciteres and Geodipsas [=Buhoma]) could perhaps be included in a subfamily Lamprophisinae. Thereafter, however, the name was not in use until reintroduced by Broadley (1998) as a tribe Lamprophiini within the family Colubridae, and by Branch (1998) and Vidal and Hedges (2002) as a subfamily Lamprophiinae. Most recently, three different nomenclatural systems have been proposed. The first (Vidal et al., 2007, Vidal et al., 2008) applied the family name Lamprophiidae to virtually all non-elapid members of the superfamily Elapoidea (excluding Micrelaps and Oxyrhabdium) and recognised a more circumscribed subfamily Lamprophiinae within this grouping. The second (Kelly et al., 2009) afforded family status to each of the major basal elapoid lineages including the Lamprophiidae, a group equivalent to the subfamily Lamprophiinae of Vidal et al., 2007, Vidal et al., 2008. In the third (Zaher et al., 2009), the family Lamprophiidae was composed of the subfamilies Pseudoxyrhophiinae and Lamprophiinae. In this latter system, the concept of Lamprophiinae is equivalent to that of Vidal et al., 2007, Vidal et al., 2008, and to the family Lamprophiidae of Kelly et al. (2009). Restricted taxon sampling and poor resolution of relationships at the base of the elapoid phylogeny in analyses based on nuclear sequence data alone (Vidal and Hedges, 2002, Vidal et al., 2007, Alfaro et al., 2008) and in those based on mixed nuclear and mitochondrial data (Vidal and Hedges, 2002, Nagy et al., 2003, Lawson et al., 2005, Vidal et al., 2008, Kelly et al., 2009, Zaher et al., 2009) mean that reciprocal monophyly of the Elapidae and the remaining Elapoidea is by no means certain. Equally tenuous is the sister relationship between Lamprophiinae and Pseudoxyrhophiinae proposed by Zaher et al. (2009), notwithstanding the putative hemipenial synapomorphies noted by these authors. Given the unresolved details of higher-order relationships within the Elapoidea, we retain the nomenclature of Kelly et al. (2009) and use the family name Lamprophiidae to refer to the elapoid clade putatively containing the following 11 genera: Bothrolycus Günther, (1 species), Bothrophthalmus Peters, 1863 (2 species), Chamaelycus Boulenger, 1919 (4 species), Dendrolycus Laurent, 1956 (1 species), Gonionotophis Boulenger, 1893 (3 species), Hormonotus Hallowell, 1857 (1 species), Lamprophis Fitzinger, 1843 (∼16 species), Lycodonomorphus Fitzinger, 1843 (∼8 species), Lycophidion Fitzinger, 1843 (∼18 species), Mehelya Csiki, 1903 (∼12 species) and Pseudoboodon Peracca, 1897 (4 species). This assemblage is equivalent to Groups 1 and 2 delineated in the influential morphological study of Bogert (1940). Monophyly of the family based on representatives from nine of the 11 genera (samples unavailable for Chamaelycus and Dendrolycus) has been demonstrated by Vidal et al. (2008), and the lineage probably has its origins in the late Eocene in Africa (Kelly et al., 2009).

Lamprophiid taxa have had a turbulent suprageneric taxonomic history. The Tribus Boaedonines of Duméril et al. (1854) and the subfamily Boodontinae of Cope (1893) both included several lamprophiid genera, and the snakes listed as Group 1 by Bogert (1940) were subsequently included in a tribe Boaedontini by Dowling (1969). Dowling and Duellman (1978) recognised the tribes Boaedontini (equivalent to Bogert’s Group 1) and Lycophidini (including Bogert’s Group 2 plus a variety of other, mainly natricine, genera), and Dowling et al. (1983) later revived Cope’s (1893) subfamily Boodontinae. McDowell (1987) recognised a subfamily Boodontinae (sensu Dowling et al., 1983) in which he provisionally included all 11 lamprophiid genera along with a disparate assortment of additional taxa. Zaher (1999) included in the Boodontinae all African ‘colubrid’ genera not clearly referable (at that time) to other suprageneric taxa, and this arrangement was adopted by Lawson et al. (2005), with slightly modified membership. However, Zaher (1999) suspected that the Boodontinae may not be monophyletic, a notion which was subsequently validated on the basis of molecular data (e.g. Vidal and Hedges, 2002, Lawson et al., 2005, Nagy et al., 2005). Only with the studies of Vidal et al. (2008) and Kelly et al. (2009) have the genera included here in the family Lamprophiidae been recognised as a distinct monophyletic assemblage and afforded suprageneric recognition.

The genus Lamprophis Fitzinger, 1843, based on the South African species Coluber aurora Linnaeus, 1754, is the type genus for the family Lamprophiidae. Many current Lamprophis species have at some time been placed in the genus Boaedon Duméril et al., 1854: Lamprophis erlangeri, Lamprophis fuliginosus, Lamprophis geometricus, Lamprophis guttatus, Lamprophis inornatus, Lamprophis lineatus, Lamprophis maculatus, Lamprophis olivaceus, and Lamprophis virgatus. However, Broadley (1983) synonymised Boaedon with Lamprophis, noting that all the characters originally used to distinguish these two genera are invalid. The content and delimitation of the genus Lamprophis were subsequently undisputed until recent studies (Vidal et al., 2008, Kelly et al., 2009) demonstrated its paraphyly and polyphyly; the genus Lycodonomorphus was shown to be embedded within a core Lamprophis clade, and the morphologically unusual Swazi Rock Snake (Lamprophis swazicus) is apparently more closely related to other lamprophiid genera than to its nominal congeners. In addition, substantial phylogenetic diversity is evident within the snakes usually referred to as L. fuliginosus (Vidal et al., 2008). Consequently, this widely-distributed and morphologically variable group will henceforth be referred to as the L. fuliginosus species complex.

Vidal et al. (2008) presents a reasonably comprehensive phylogeny for the family Lamprophiidae (their subfamily Lamprophiinae), but neither they nor Kelly et al. (2009) specifically addressed taxonomic implications of the phylogenetic results. In this study we extend current phylogenetic understanding via analysis of an expanded lamprophiid taxon sample, and we also take formal taxonomic action where this is deemed justified by the phylogenetic results.

Section snippets

Taxon sampling and laboratory protocols

Our taxon set comprised 77 terminals (individual samples), including 28 of the approximately 68 recognised lamprophiid species from nine of the 11 genera, and six outgroup taxa from throughout the remainder of the Elapoidea (Table 1). Our mitochondrial data set included sequences from the cytochrome b (cyt b, 1100 bases) and NADH dehydrogenase subunit 4 genes (ND4, 693 bases), and 156 bases from three transfer RNA (tRNA) genes flanking the 3′ end of the ND4 gene (tRNAHis, tRNASer, tRNALeu). Our

Alignment and genetic distances

Alignment was unambiguous for all protein-coding genes, and no frame-shift mutations or premature stop codons were detected. One triplet gap was required for preservation of homology in the cyt b alignment, one triplet and one sextuplet gap were required for c-mos, and for tRNA 10 gaps were required ranging from one to five bases in length. The full data set comprised 2519 characters; 1224 variable and 1031 parsimony-informative characters inclusive of outgroups, and 1112 variable and 979

A new genus for ‘Lamprophis’ swazicus

In agreement with recent studies (Vidal et al., 2008, Kelly et al., 2009), our results clearly demonstrate that L. swazicus (the Swazi Rock Snake) is misplaced in the genus Lamprophis. Since its original description (Schaefer, 1970), the generic placement of L. swazicus has been problematic. Schaefer (1970) noted that the new species appeared intermediate between the then recognised house snake genera Boaedon and Lamprophis, and chose to place it within the latter. Visser, 1978, Visser, 1979,

Acknowledgments

We gratefully acknowledge the Tanzania Commission for Science and Technology, the Tanzania Wildlife Research Institute and the Rwanda Office of Tourism and National Parks for providing collecting permits; Graham Alexander, Mike Bates, Marius Burger, Keshni Gopal, Lauretta Mahlangu, Devon Massyn, Tony Phelps, Don Schultz and Krystal Tolley for supplying tissue samples; Nick Vidal for kindly providing access to many relevant DNA sequences prior to their deposition in public data bases; the

References (57)

  • C.M. Bogert

    Herpetological results of the Vernay Angola expedition. Part 1. Snakes, including an arrangement of the African Colubridae

    Bull. Am. Mus. Nat. Hist.

    (1940)
  • Bourgeois, M., 1968. Contribution à la morphologie comparée du crâne des ophidiens de l’Afrique Centrale. Publ. Univ....
  • W.R. Branch

    A Field Guide to the Snakes and other Reptiles of Southern Africa

    (1998)
  • M.C. Brandley et al.

    Partitioned bayesian analyses, partition choice, and the phylogenetic relationships of scincid lizards

    Syst. Biol.

    (2005)
  • D.G. Broadley

    FitzSimons’ Snakes of Southern Africa (Revised ed.)

    (1983)
  • D.G. Broadley

    Fitzsimon’s Snakes of Southern Africa

    (1990)
  • Broadley, D.G., 1998. Introduction to reptilia. In: Schmidt, K.P., Noble, G.K., 1919–1923. Contributions to the...
  • F.T. Burbrink et al.

    Mitochondrial DNA phylogeography of the polytypic North American rat snake (Elaphe obsoleta): a critique of the subspecies concept

    Evolution

    (2000)
  • T.A. Castoe et al.

    Data partitions and complex models in Bayesian analysis: the phylogeny of gymnophthalmid lizards

    Syst. Biol.

    (2004)
  • J.-P. Chippaux

    Les serpents d’Afrique occidentale et centrale

    (2001)
  • E.D. Cope

    Prodromus of a new system of the non-venomous snakes

    Am. Nat.

    (1893)
  • H.G. Dowling

    Relations of some African colubrid snakes

    Copeia

    (1969)
  • H.G. Dowling et al.

    Systematic Herpetology: A Synopsis of Families and Higher Categories

    (1978)
  • H.G. Dowling et al.

    Biochemical evaluation of colubrid snake phylogeny

    J. Zool.

    (1983)
  • Duméril, A.M.C., Bibron, G., Duméril, A.H.A., 1854. Erpétologie générale ou histoire naturelle complète des reptiles....
  • H.J. Dumont

    On the validity of the generic name Simocephalus Schoedler, 1858 (Cladocera)

    Crustaceana

    (1977)
  • J.S. Farris et al.

    Constructing a significance test for incongruence

    Syst. Biol.

    (1995)
  • J. Felsenstein

    Confidence limits on phylogenies: an approach using the bootstrap

    Evolution

    (1985)
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