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Herpetological Journal FULL PAPER Volume 29 (July 2019), 162-172 Herpetological Journal FULL PAPER https://doi.org/10.33256/hj29.3.162172 Published by the British Phylogenetic relationships and origin of the rattlesnakes Herpetological Society of the Gulf of California islands (Viperidae: Crotalinae: Crotalus) Eduardo Ruiz-Sanchez1, Gustavo Arnaud2, Oscar Roberto Cruz-Andrés2 & Francisco Javier Garcia-De León3 1 Departamento de Botánica y Zoología, Centro Universitario de Ciencias Biológicas y Agropecuarias, Universidad de Guadalajara, Camino Ing. Ramón Padilla Sánchez 2100, Nextipac, Zapopán, Jalisco 45200, Mexico 2 Centro de Investigaciones Biológicas del Noroeste, S.C. Instituto Politécnico Nacional 195, Col. Playa Palo de Santa Rita, La Paz, B.C.S. 23090, Mexico 3 Laboratorio de Genética para la Conservación, Centro de Investigaciones Biológicas del Noroeste, Instituto Politécnico Nacional 195, Playa Palo de Santa Rita, La Paz, B.C.S. 23096, Mexico The islands of the Gulf of California are divided into three categories – oceanic, continental, and landbridge – and were formed from the Middle Miocene to the Holocene. The species of the Crotalus genus are an important ecological element of the endemic fauna of these islands. This study is the first to include several island-endemic species in a phylogenetic framework. We seek to understand the phylogenetic relationships among these species, and in particular, whether these species are more related to the Baja California peninsula or continental Mexican species, and whether the divergence times for these relationships are consistent with the formation of the islands. We performed a phylogenetic analysis and estimated divergence times using Bayesian inference and two mitochondrial 12S and 16S genes. The analyses show a new relationship between Crotalus angelensis and C. pyrrhus. Crotalus lorenzoensis was nested with C. ruber individuals, making this species a paraphyletic species. A novel relationship was also detected in thatC. estebanensis was sister to C. basiliscus. The divergence time for all island-endemic Crotalus species is consistent with the formation of these islands. In addition, the insular species are related to their congeners in the Baja California peninsula or mainland Mexico. Keywords: Baja California Peninsula; Bayesian inference; island-endemic; mtDNA; rattlesnakes INTRODUCTION of the peninsula as it moved north-west. The landbridge islands are the commonest and youngest of all the he Baja California peninsula began to form during islands in the Gulf of California and were connected to Tthe Middle Miocene due to the expansion process Baja California or mainland Mexico, but for the most part, that occurred between the Pacific and North American were cut off by a rise in the sea level (Grismer, 2002). tectonic plates. As far as we know, the peninsula was These three types of islands can be separated into three formed progressively at the end of the Pliocene and the regions: the northern, central midriff, and southern gulf beginning of the Pleistocene, approximately 2.58 million areas (Carreño & Helenes, 2002). years ago (Smith, 1991; Riddle et al., 2000a; Holt et al., The northern islands were formed by sedimentation of 2000; Oskin & Stock, 2003; Wood et al., 2008; Murphy & sediment delivery from the Colorado River. Some of these Aguirre-León, 2002; Murphy & Méndez de la Cruz, 2010). islands were formed in the Holocene, while the rest were This also led to the formation of the Gulf of California the result of volcanic activity during the early Pleistocene (GC). (Carreño & Helenes, 2002). The central islands emerged The Gulf of California has a complex geological during the middle to late Miocene (15-10 and 10-5 Ma). history with two stages of formation: the first during Those islands were uplifted due to the many faults in the Miocene and the second in the Pliocene (Carreño & the region from the Pleistocene to the Holocene. Finally, Helenes, 2002). The islands constitute one of the Gulf of volcanic activity, granitic rock or oceanic sediments from California’s most interesting features and are classified the Pliocene formed the southern islands. Altogether, this into three types: oceanic, continental, and landbridge led to the formation of about 100 islands and islets, most (Grismer, 2002). The oceanic islands of the GC have of which were colonised by species of flora and fauna never been connected to Baja California (BC) or mainland from Baja California and mainland Mexico. According Mexico. The continental islands were once connected to to Grismer (2002), there are 161 species of native and the Baja California peninsula and/or mainland Mexico but non-native species of herpetofauna in the Baja California became separated as a result of tectonic displacements peninsula and the Pacific and GC islands. Four of these along coastal fault zones, and broke off the trailing edge species are salamanders, 13 frogs, 4 turtles, 84 lizards, Correspondence: Francisco Javier Garcia-De León ([email protected]) ; Gustavo Arnaud ([email protected]) 16234 Phylogeny of island-endemic Crotalus species Figure 1. Distribution of species of rattlesnakes from the Gulf of California islands, the California peninsula, and mainland Mexico. Symbols represent sampling locations and indicate the corresponding species. and 57 snakes. Among the snakes, the Viperidae family is Table 1. Crotalus species present in the Baja California represented by 17 Crotalus species (Grismer, 2002; Meik peninsula (BCP), Gulf de California Islands (GCI), Pacific et al., 2018). Ten of these are island-endemic and one is Islands (PI), Mainland Mexico (MM), and the United States endemic to the peninsula (Table 1; Grismer, 2002; Ernst of America (USA), based on Grismer (2002), Ernst and Ernst & Ernst, 2012; Meik et al., 2018). Five species are shared (2012), and Meik et al. (2018). between California and the Baja California peninsula (C. atrox, C. cerastes, C. mitchellii, C. oreganus, and C. ruber), Species BCP GCI PI MM USA and four island species are shared between the United Crotalus angelensis X States and mainland Mexico (C. atrox, C. cerastes, C. Crotalus atrox X X X X mitchellii, and C. molossus; Ernst & Ernst, 2012). Crotalus catalinensis¹ X Mexico is considered the center of diversification Crotalus caliginis¹ X of Crotalus snakes, since about 92 % of the species Crotalus cerastes X X X X of this group are found in the country (Klauber, 1972; Crotalus enyo² X X X Armstrong & Murphy, 1979; Greene, 1997; Flores- Crotalus estebanensis¹ Villela & Canseco-Márquez, 2004; Paredes-García et al., X 2011). The Crotalus genus probably originated during Crotalus lorenzoensis¹ X the Middle Miocene (Bryson et al., 2010). The Sierra Crotalus pyrrhus X X X X Madre Occidental and the Mexican Plateau have the Crotalus mitchellii X X X X X highest diversity of Crotalus species (Campbell & Lamar, Crotalus molossus X X X 2004), with the former considered the ancestral area for Crotalus oreganus X X the genus (Place & Abramson, 2004). Crotalus species in Crotalus polisi¹ X mainland Mexico and Baja California may be the ancestors Crotalus ruber X X X X of the endemic island species. However, to date there has Crotalus thalassoporus¹ X been no single phylogenetic hypothesis that includes all Crotalus tortugensis¹ X the Crotalus species endemic to the islands. Crotalus tigris X X X Previous molecular phylogenetic analyses using four mitochondrial genes (12S, 16S, ND4, and cytB) and 61 Total 7 15 4 6 8 ¹ Island-endemic, ² BCP-endemic 16335 E. Ruiz-Sanchez et al. Figure 2. Crotalus species sampled in this study. 1. C. oreganus, 2. C. angelensis, Ángel de la Guarda Island 3. C. catalinensis, Santa Catalina Island, 4. C. enyo, 5. C. ruber, 6. C. estebanensis, San Esteban Island, 7. C. lorenzoensis, San Lorenzo Island, 8. C. mitchellii, 9. C. enyo (La Paz). 10. C. cerastes, 11. C. pyrrhus, El Muerto Island, 12. C. atrox, Tortuga Island. Pictures by Gustavo Arnaud, Francisco Javier García-De León and Fernando Pozas. Crotalinae species, of which four were Crotalus species, and C. viridis helleri from Santa Catalina Island (USA), found that this genus was monophyletic and sister to Ashton & de Queiroz (2001) found strong support for the the Sistrurus genus (Parkinson et al., 2002). Murphy separation of C. viridis from C. oreganus. et al. (2002) conducted a more extensive phylogenetic To date, not all Crotalus island species in the GC and analysis using 27 Crotalus species. In their sampling, they the Pacific have been included in a phylogenetic study. included Crotalus catalinensis from Santa Catalina Island, Therefore, here we include all the insular Crotalus species C. atrox from Santa Cruz Island and (C. tortugensis = C. represented by more than one individual, except the atrox) from Tortuga Island. They found sister relationships newly described C. polisi and C. thalassoporus species between C. catalinensis and C. ruber and (C. tortugensis = (Meik et al., 2018), with the aim of answering the following C. atrox) was nested in a clade with two C. atrox species, questions: 1) “What phylogenetic relationships exist and was sister to C. atrox from Santa Cruz Island. Castoe between insular species and other Crotalus species?”, 2) et al. (2007) performed a population study of C. atrox and “Are insular species more closely related to species from found that (C. tortugensis = C. atrox) and C. atrox from Baja California or species from mainland Mexico?”, and 3) Santa Cruz Island are nested within mainland lineages “What are the divergence times of the insular species
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