African Herald Snakes, Crotaphopeltis, Show Population Structure for a Widespread Generalist but Deep Genetic Divergence for Forest Specialists

Received: 9 May 2019 | Revised: 12 November 2019 | Accepted: 14 November 2019 DOI: 10.1111/jzs.12361

ORIGINAL ARTICLE

African Herald snakes, Crotaphopeltis, show population structure for a widespread generalist but deep genetic divergence for forest specialists

1South African National Biodiversity Institute, Kirstenbosch Research Centre, Claremont, South Africa 2Department of Botany & Zoology, Stellenbosch University, Matieland, South Africa 3Port Elizabeth Museum (Bayworld), Port Elizabeth, South Africa 4Department of Zoology, Nelson Mandela University, Port Elizabeth, South Africa 5Department of Biological Sciences, University of Texas at El Paso, El Paso, TX, USA 6African Amphibian Conservation Research Group, Unit for Environmental Sciences and Management, North-West University, Potchefstroom, South Africa 7Flora Fauna & Man, Ecological Services Ltd., Tortola, British Virgin Islands 8School of Natural Resource Management, Nelson Mandela University, George, South Africa 9National Geographic Okovango Wilderness Project, The Wild Bird Trust, Parktown, South Africa 10Centre for Ecological Genomics and Wildlife Conservation, University of Johannesburg, Auckland Park, South Africa

Correspondence Hanlie M. Engelbrecht, School of Animal, Abstract Plant, and Environmental Sciences, The African colubrid snake genus Crotaphopeltis currently comprises six species and University of the Witwatersrand, PO Wits, Johannesburg, Gauteng 2050, South Africa. occurs throughout sub-Saharan Africa. The most widespread of these, Crotaphopeltis Email: [email protected] hotamboeia, inhabits most biomes, aside from rainforest and hyper-arid regions, and

Funding information its catholic niche has presumably facilitated substantial gene flow. Despite this, the Andrew W. Mellon Foundation; Percy geographical range is large enough that ecological or physical barriers might exist, Sladen Memorial Fund; IUCN/SSC Amphibian Specialist Group Seed Grant; K. facilitating allopatric diversification. In contrast, most of the other species are habitat Reed, M.D.; National Science Foundation, specialists with limited distributions (e.g., Crotaphopeltis tornieri) and would be ex- Grant/Award Number: DEB-1145459; National Geographic Society Committee pected to show strong genetic structure. We therefore examined species boundaries for Research and Exploration, Grant/Award within Crotaphopeltis in a phylogenetic context using five markers (16S, cyt b, ND4, Number: 9281-13 and 8556-08; National Research Foundation of South Africa, Grant/ c-mos, and R AG-1) for four of the six species. Species delimitation methods included Award Number: CPRR-UID97226 and two coalescent-based and one barcoding approach. Widespread geographical sam- IPRR-UID85413; Department of Biology at Villanova University; South African National pling of C. hotamboeia allowed examination of genetic structuring across its range. Biodiversity Institute The species status of Crotaphopeltis barotseensis, C. degeni, and C. hotamboeia was confirmed, whereas the Afromontane species C. tornieri comprised two candidate species. Crotaphopeltis hotamboeia did not show cryptic speciation, although its phy- logeographic structure corresponded with the spatiotemporal pattern of the African savanna. Our results show how the heterogeneous African environment could influ- ence genetic partitioning of habitat specialist and generalist species at broad geographical scales.

Contributing authors: William R. Branch (deceased), Eli Greenbaum ([email protected]), Marius Burger ([email protected]), Werner Conradie ([email protected]), Krystal A. Tolley ([email protected]).