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Genus: Aristelliger) The Pennsylvania State University The Graduate School Eberly College of Science CRYPTIC DIVERSITY, EVOLUTION, AND BIOGEOGRAPHY OF CARIBBEAN CROAKING GECKOS (GENUS: ARISTELLIGER) A Thesis in Biology by Tiffany Loren Cloud © 2013 Tiffany Loren Cloud Submitted in Partial Fulfillment of the Requirements for the Degree of Master of Science May 2013 ii The thesis of Tiffany Loren Cloud reviewed and approved* by the following: S. Blair Hedges Professor of Biology Thesis Adviser Charles R. Fisher Professor of Biology, Assistant Department Head for Graduate Education Tracy Langkilde Associate Professor of Biology *Signatures are on file in the Graduate School. iii Abstract The sphaerodactylid gecko genus Aristelliger (Caribbean croaking geckos) currently contains eight described species, all found on Caribbean islands. Mitochondrial DNA (mtDNA) sequence data from 106 specimens representing all eight currently recognized species were used to evaluate the relationships of the species within the genus. The molecular phylogeny of the genus is inconsistent with the current species-level taxonomy. Species delimitation methods indicate that there are as many as 24 species, hidden within the eight currently described species. This was especially true of Aristelliger praesignis (Jamaican Croaking Gecko) which has 10 clades of potential species-status, eight of which are in Jamaica, showing deep genetic divergences. Further support that at least six of these clades represent cryptic species comes from the consistency with which most clades can be differentiated from each of the other clades based on morphological characters. In addition, two clades are sympatric and syntopic at Port Antonio, Portland Parish, Jamaica. Another two clades are nearly sympatric, separated by only about 0.75 km at Port Maria and Cabarita Island, St. Mary Parish, Jamaica. In addition to the high levels of cryptic diversity found within Jamaica, A. georgeensis (St. George Island Gecko)—the only member of this genus found on the mainland—is nested within a clade of A. praesignis from Port Antonio, and is the most recent of the clades to diverge, about 1.5 million years ago (Ma). Based on molecular divergence time estimation and geology, it is likely that this genus originated on Hispaniola between 37 Ma and 23 Ma. From there, a lineage invaded Jamaica giving rise to A. praesignis. There have been three dispersals out of Jamaica giving rise to populations or species elsewhere: two out of northern Jamaica, and one very recently from southwestern Jamaica. iv Table of Contents List of Figures……………………………………………………………………..…..………...v List of Tables……………………………………………………………………………..….….vi Introduction …………………………………………………………………………………......1 Materials and Methods………………………………………………………………..….......11 Results…………………………………………………………………………………….…....17 Discussion………………………………………………………………………………….…..27 References……………………………………………………………………………………..37 v List of Figures Figure 1—Bayesian inference tree showing relationships within Aristelliger......……………...…20 Figure 2— Maximum likelihood tree showing relationships within Aristelliger ……………….....21 Figure 3— Portion of maximum likelihood tree showing relationships within A. praesignis with a map of Jamaica showing the localities of the Jamaican clades……………………....22 Figure 4—Molecular timetree for the genus Aristelliger………………………………………...…..23 Figure 5—Neighbor Joining tree showing groups defined by ABGD………………..…….......….24 vi List of Tables Table 1— Most useful traits for distinguishing between each pair of clades……………………..25 Table 2—Weighted and Unweighted Classification Scores…………………...……..………….....26 1 Introduction The incorporation of molecular techniques in taxonomy has revolutionized species discovery (Bickford et al., 2007; Nagy et al., 2012). Two of the past five years have been record-breaking for the number of reptile species described in a single year: 166 species in 2007 and 168 species in 2012 (Uetz, 2013). There were only 3 other years in history that there were over 100 species of reptiles described: 1758, 1854 and 1863 (Uetz, 2013). In addition, 3,076 species of amphibians have been described since 1985, a 75% increase (AmphibiaWeb), and 408 new species of mammals were discovered between 1993 and 2008, a 10% increase (Ceballos & Ehrlich, 2009). The identification of cryptic species has played a major role in the increased rate of species discovery. Cryptic species are species that have been lumped under one species name due to being, at least superficially, indistinguishable morphologically (Beheregaray & Caccone, 2007; Pfenninger & Schwenk, 2007; Barata, Carranza & Harris, 2012). The use of molecular data has been responsible for many of these discoveries. Before 1989, when PCR was first used in evolutionary biology (Kocher et al., 1989), very few studies mentioned cryptic species. However, the number of such studies has risen exponentially since then and by 2005 over 20% of studies mentioned cryptic species (Bickford et al. 2007). Within mammals, 60% of the new species are considered cryptic species (Ceballos & Ehrlich, 2009). Even charismatic, widely studied organisms have been shown to harbor cryptic species, such as giraffes (Brown et al., 2007), elephants (Roca et al., 2001), and hammerhead sharks (Pinhal et al., 2012). Furthermore, cryptic species are not limited to a certain region or environment and have been found in developed countries that have been well-studied such as Australia, 2 Europe, and North America (Kiefer & Veith, 2001; Rissler & Apodaca, 2007; Oliver et al., 2009; Manthey, Klicka, & Spellman, 2011; Smith et al., 2011; Yang et al., 2012). There are certain natural history traits that seem to be associated with having higher levels of cryptic diversity. Organisms that are less dependent on visual cues in selecting mates, using instead nonvisual mating cues such as acoustic calls or pheromones tend to have a greater number of cryptic species (Bickford et al. 2007; Hoskin & Higgie, 2010; Clare et al., 2011). In addition, certain environmental factors can impose strong selection on maintaining the ancestral morphology. For example, symbionts specialized to specific host tend to harbor cryptic species due to strong selection to maintain the traits that enable them to infiltrate the host’s body or society (Schönrogge et al., 2002; Locke, McLaughlin, & Marcogliese, 2010). Extreme environments, such as; subterranean, arctic tundra or deep sea environments also tend to harbor greater numbers of cryptic species (Lefébure et al., 2006; Bickford et al., 2007; García-Machado, 2011). Genus: Aristelliger The genus Aristelliger, commonly known as the Croaking Gecko or the Caribbean Gecko, is currently comprised of eight recognized species (Diaz & Hedges, 2009). The members of this genus are found exclusively in the Caribbean and along the east coast of Central America (Bauer & Russell, 1993a). The genus is characterized by the following morphological characteristics: skin that is easily torn, mottled with browns and tans, small granular scales, vertical pupils, friction pads on at least two digits, bones in the hemipenes, oil droplets in rods, undivided lamellae, croaking call, and all 3 digits having claws (Cope,1862; Underwood, 1954; Bauer & Russell, 1993a; Diaz & Hedges, 2009). Members of this genus are primarily arboreal. They are often found in trees; living, dead, or rotting and often under the bark. They are commonly associated with Coconut Palms (Cocos) and Fig trees (Ficus) but this varies by species. In addition, they are found in palm trash and under rocks (Noble & Klingel, 1932; Thomas, 1966; Schwartz & Crombie, 1975; Henderson & Powell, 2009). They also take advantage of man-made structures, such as on thatched roofs, in rafters, in crevices of walls or on fences (Schwartz & Henderson, 1991; Lee, 1996; Henderson & Powell, 2009). At night they are quite vocal (Dunn & Saxe, 1950; Hecht, 1952; Schwartz & Henderson, 1991). Their diet is primarily composed of arthropods (Henderson & Powell,1999), though Aristelliger cochranae females are known to eat gecko eggs and hatchlings (Gifford et al., 2000), A. georgeensis—anoline lizards (Dunn & Saxe, 1950; Lee, 1996) and A. lar will eat berries and flowers (Burns et al., 1992; Henderson & Powell, 2009), in addition to arthropods. Females lay a single egg per clutch (Kluge, 1967; Daza & Bauer, 2012) up to twice a year (Hecht, 1952). The eggs are typically sticky and are laid on trees; sometimes in the open or in hollows and under the bark; in crevices between rocks; or on the backs of fronds (Henderson & Powell, 2009). The eggs can be laid singly or in a communal nest and are incubated for about 3 months (Barbour, 1910; Noble and Klingel, 1932; Hecht, 1952). There are two subgenera within Aristelliger distinguishable by size and number of friction pads. The smaller subgenus is Aristelligella (Noble and Klingel, 1932), which has a maximum snout-vent length of 63 mm and friction pads on three fingers and two toes. 4 The subgenus Aristelliger (Cope, 1862) is much larger, with a maximum SVL of 135 mm. They have friction pads on only one finger and one toe (Hecht, 1951; Bauer & Russell 1993a; Diaz & Hedges, 2009). Subgenus: Aristelligella Between 1931 and 1933 three of the four species belonging to the subgenus Aristelligella were described. The first to be described was Cochran’s croaking gecko, Aristelliger cochranae, which was described in 1931 by Grant. This species is found on Navassa Island off the coast of Haiti. Grant named it in honor of Doris Cochran who was the
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