Unexpected Shallow Genetic Divergence in Turks Island Boas (Epicrates C. Chrysogaster) Reveals Single Evolutionarily Significant Unit for Conservation Author(S) :R
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Unexpected Shallow Genetic Divergence in Turks Island Boas (Epicrates c. chrysogaster) Reveals Single Evolutionarily Significant Unit for Conservation Author(s) :R. Graham Reynolds, Glenn P. Gerber, and Benjamin M. Fitzpatrick Source: Herpetologica, 67(4):477-486. 2011. Published By: The Herpetologists' League DOI: URL: http://www.bioone.org/doi/full/10.1655/HERPETOLOGICA- D-11-00014.1 BioOne (www.bioone.org) is a a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/ terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. Herpetologica, 67(4), 2011, 477–486 E 2011 by The Herpetologists’ League, Inc. UNEXPECTED SHALLOW GENETIC DIVERGENCE IN TURKS ISLAND BOAS (EPICRATES C. CHRYSOGASTER) REVEALS SINGLE EVOLUTIONARILY SIGNIFICANT UNIT FOR CONSERVATION 1,3 2 1 R. GRAHAM REYNOLDS ,GLENN P. GERBER , AND BENJAMIN M. FITZPATRICK 1Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, TN 37996, USA 2Institute for Conservation Research, San Diego Zoo Global, Escondido, CA 92027, USA ABSTRACT: The Turks Island Boa (Epicrates c. chrysogaster) is endemic to the Turks and Caicos Islands and is currently known from only 11 islands. The subspecies has likely been extirpated from several islands in its historic range, and all remaining populations are threatened with extirpation owing to habitat loss, introduced feral predators, malicious killing, and vehicle strikes. To assist conservation efforts, we undertook a genetic analysis of 53 individual E. c. chrysogaster, representing five island populations, with the goal of identifying existing population structure and genetic diversity. For each snake sampled, we sequenced one mitochondrial and two nuclear genes, resulting in 1591 bp of sequence, and screened nine microsatellite loci. All individuals were found to be monomorphic at the four microsatellite loci that amplified, and only three individuals were found to vary (by a single nucleotide polymorphism) in either nuclear gene. Nine mitochondrial haplotypes were found, with a maximum sequence divergence of ,1%. Taken together, these data indicate shallow genetic divergence in this subspecies, possibly owing to a lack of historical population structure and small population size when the Turks and Caicos Banks were each single islands during the last glacial maximum. Epicrates c. chrysogaster appears to represent a single evolutionarily significant unit, a significant finding suggesting that conservation strategies focusing on ecologically intact populations might be more appropriate than alternate strategies involving near-impossible reversal of declining populations on heavily disturbed islands. In addition, reintroduction programs would likely not disrupt any significant historical population structure. Key words: Boinae; Caribbean; Epicrates chrysogaster; Population structure; Snake; Turks and Caicos Islands; West Indies KNOWLEDGE of standing genetic variation andRedig,2001),GrayWolves(Canis lupus within and between populations of species is [Fritts et al., 1997]), Bald Eagles (Haliaeetus important in designing conservation strategies lecuocephalus [Nye, 1988]), Seychelles Kestrels (Allendorf and Luikart, 2007; Caballero et al., (Falco areaus [Watson, 1989]), and Turks and 2010; Frankham, 2006; Frankham et al., Caicos Rock Iguanas (Cyclura c. carinata 2002). When populations are separated from [Gerber, 2007]). However, many caution against each other, as in island archipelagoes, pro- translocations that might disrupt natural genetic cesses such as mutation, genetic drift, gene structure (Allendorf and Luikart, 2007; Avise, flow, local extinction, and recolonization 2004; Storfer, 1999). might dramatically influence the apportioning The West Indies is one of the world’s of genetic variation within geographically biodiversity hotspots (Myers et al., 2000; structured populations (Slatkin, 1987; Wade Smith et al., 2005). The region has a diverse and McCauley, 1988; Whitlock and McCauley, herpetofaunal assemblage and these species 1990; Wright, 1977). Thus, understanding the are of particular conservation concern owing to distribution of genetic variation in an archipe- their vulnerability to anthropogenic threats, lagic species can shed light on evolutionary especially habitat destruction and the intro- processes operating in that system and might be duction of invasive mammalian predators such used to develop conservation management as House Cats (Felis catus), Small Indian strategies that minimize disruption of those Mongoose (Herpestes javanicus auropuncta- processes. In particular, translocation has been tus), and Black Rats (Rattus rattus), among an important tool in the recovery of high-profile others (Corke, 1992; Hailey et al., 2011; species such as Peregrine Falcons (Falco Iverson, 1978; Smith et al., 2005; Tolson and peregrinus [Cade and Burnham, 2003]; Tordoff Henderson, 2006). The Turks and Caicos Islands (TCI), located at the southern terminus 3 CORRESPONDENCE: e-mail, [email protected] of the Bahama Archipelago, contain a unique 477 478 HERPETOLOGICA [Vol. 67, No. 4 FIG. 1.—Map of the Turks and Caicos Islands illustrating sampling locations (December 2007–March 2010) of Epicrates c. chrysogaster. Inset map shows the location of the Turks and Caicos Islands within the greater Caribbean region. Outlines indicate the approximate extent of the Caicos and Turks banks. Haplotype map is the TCS statistical parsimony network overlaid onto a map of the Turks and Caicos Islands. Circles represent individual haplotypes, the size of which corresponds to the number of sequences each haplotype contains. Circles are divided and shaded to show the proportion of each island population within each haplotype, and each island is assigned a unique shading pattern. Small black circles indicate unobserved haplotypes. Haplotypes are connected with a 95% CL. endemic herpetofauna (Reynolds, 2011; Rey- islands, including Grand Turk and South nolds and Niemiller, 2010a) that is threatened Caicos and populations on major islands are by increasing development and population likely in a sharp decline (Reynolds, 2011). growth. The TCI consist of more than 200 Turks Island Boas face numerous threats, islands, ranging in size from ,1hato including development and associated habitat .12,000 ha, distributed on two shallow banks loss, introduced predators, direct persecution, (Fig. 1). The Turks and Caicos Banks are 150- and vehicular traffic, and very little is published million-yr-old sediment and limestone plat- about the ecology, distribution, and natural forms that have remained near the ocean history of this species (Reynolds, 2011; Rey- surface due to reef building. Various portions nolds and Niemiller, 2010a). of the banks have been alternately emergent Other reptiles in the region, such as the and inundated throughout this time, though Turks and Caicos Rock Iguana, are facing both banks were fully emergent within the last similar threats and extirpations (Gerber and 8000–15,000 yr. The two banks are separated Iverson, 2000; Iverson, 1978; Reynolds, 2011). by the narrow and deep Turks Island Passage As a result, they are being intensively managed and have never been joined, and rising sea and translocated to some of the outer islands levels since the Wisconsin glacial maximum that are free from introduced predators and partitioned each bank into the present islands development (Gerber, 2007). To help develop (Fairbanks, 1989; Lighty et al., 1982; Welch conservation strategies for Epicrates, we sam- et al., 2004). The Turks Island Boa, Epicrates pled boas from islands on the Turks Bank and c. chrysogaster, is an endemic nocturnal– the Caicos Bank to assess standing genetic crepuscular boine and the largest native diversity among populations and to investigate terrestrial carnivore in the TCI. Boas have whether separate evolutionarily significant been reported from 11 islands in the TCI, units (ESUs; Crandall et al., 2000; Mortiz, while extirpations have occurred on several 1994; Ryder, 1986; Waples, 1991), or populations December 2011] HERPETOLOGICA 479 TABLE 1.—Sampling locations in the Turks and Caicos Islands (December 2007–March 2010) and sampling effort used to obtain tissue samples of Epicrates c. chrysogaster used in this analysis. Effort is represented as person-hours (p/h), the amount of time spent searching by all individuals that day. Two additional islands (Long Cay and Little Ambergris Cay) where Epicrates is thought to occur (Reynolds, 2011) were also searched but yielded no specimens. Note that four individuals sampled from Providenciales and five individuals sampled from North Caicos were wild-caught captives being held for educational purposes, with known locality information. Island Date(s) Effort Captures Big