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An Incipient Invasion of Brown Anole Lizards (Anolis Sagrei) Into Their Own Native Range in the Cayman Islands: a Case of Cryptic Back-Introduction

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An Incipient Invasion of Brown Anole Lizards (Anolis Sagrei) Into Their Own Native Range in the Cayman Islands: a Case of Cryptic Back-Introduction Biol Invasions DOI 10.1007/s10530-017-1432-2 INVASION NOTE An incipient invasion of brown anole lizards (Anolis sagrei) into their own native range in the Cayman Islands: a case of cryptic back-introduction Jason J. Kolbe . Johanna E. Wegener . Yoel E. Stuart . Ushuaia Milstead . Katherine E. Boronow . Alexis S. Harrison . Jonathan B. Losos Received: 29 July 2016 / Accepted: 31 March 2017 Ó Springer International Publishing Switzerland 2017 Abstract Human-mediated dispersal has reshaped Cayman, have been found on Cayman Brac where the distribution patterns and biogeographic relationships native A. sagrei have yellow dewlaps. Our analysis of for many taxa. Long-distance and over-water dispersal microsatellite data shows strong population-genetic were historically rare events for most species, but now structure among the three Cayman Islands, but also human activities can move organisms quickly over evidence for non-equilibrium. We found some long distances to new places. A potential consequence instances of intermediate multilocus genotypes (pos- of human-mediated dispersal is the eventual reintro- sibly 3–9% of individuals), particularly between duction of individuals from an invasive population Grand Cayman and Cayman Brac. Furthermore, back into their native range; a dimension of biological analysis of dewlap reflectance data classified six invasion termed ‘‘cryptic back-introduction.’’ We males sampled on Cayman Brac as having red dewlaps investigated whether this phenomenon was occurring similar to lizards from Grand Cayman and Little in the Cayman Islands where brown anole lizards Cayman. Lastly, one individual from Cayman Brac (Anolis sagrei) with red dewlaps (i.e., throat fans), had an intermediate microsatellite genotype, a red either native to Little Cayman or invasive on Grand dewlap, and a mtDNA haplotype from Grand Cayman. This mismatch among genetic and phenotypic data strongly suggests that invasive A. sagrei from Grand Electronic supplementary material The online version of Cayman are interbreeding with native A. sagrei on this article (doi:10.1007/s10530-017-1432-2) contains supple- mentary material, which is available to authorized users. Cayman Brac. To our knowledge, this is the first evidence of cryptic back-introduction. Although we J. J. Kolbe (&) Á J. E. Wegener Á U. Milstead demonstrate this phenomenon is occurring in the Department of Biological Sciences, University of Rhode Cayman Islands, assessing its frequency there and Island, 120 Flagg Road, Kingston, RI 02881, USA e-mail: [email protected] prevalence in other systems may prove difficult due to the need for genetic data in most instances. Cryptic Y. E. Stuart Á K. E. Boronow Á A. S. Harrison Á back-introductions may eventually provide some J. B. Losos insight into how lineages are changed by the invasion Department of Organismic and Evolutionary Biology and Museum of Comparative Zoology, Harvard University, process and may be an underappreciated way in which 26 Oxford Street, Cambridge, MA 02138, USA invasive species impact native biodiversity. Present Address: Keywords Admixture Á Dewlap Á Microsatellites Á Y. E. Stuart Department of Integrative Biology, University of Texas at Nuclear-mitochondrial mismatch Á Reintroduction Á Austin, 2401 Speedway, Austin, TX 78712, USA Reproductive isolation 123 J. J. Kolbe et al. Introduction and relatively remote islands in the western Car- ibbean. Subsequently, A. sagrei differentiated into In this era of widespread human-mediated dispersal, the yellow-dewlapped endemic subspecies A. s. geographic distance is no longer a barrier to movement luteosignifer on Cayman Brac and the red-dewlapped for many species. Exotic species introductions have A. s. sagrei on Little Cayman (Schwartz and altered fundamental biogeographic patterns such as Henderson 1991); the dewlap is an extendable throat species-area and species-isolation relationships fan used for communication in anoles (Losos 2009). (MacArthur and Wilson 1963; Sax et al. 2005). For However, A. sagrei failed to colonize the third of the example, colonization by exotic Anolis lizards in the Cayman Islands, Grand Cayman, which is loca- Caribbean has altered pre-invasion biogeographic ted *100 km farther to the southwest of the other patterns (Losos and Schluter 2000), effectively reduc- Cayman Islands from Cuba. That is, until the early ing geographic isolation among islands and flattening 1980s when a red-dewlapped form of A. sagrei the negative species-isolation relationship for anoles became established on Grand Cayman, thereby (Helmus et al. 2014). Long-distance colonization accomplishing a long-distance dispersal event that events due to human activity can bring together failed to occur naturally. Grand Cayman populations evolutionarily distinct lineages that in some instances resulted from a human-mediated introduction of have been separated for millions of years (e.g., Kolbe genetically admixed lizards, not from its native et al. 2004). Novel interactions among these lineages range, but from established non-native populations could reshape existing ecological communities and in south Florida (Minton and Minton 1984; Kolbe alter patterns of species diversity (e.g., Stuart et al. et al. 2004, 2008;Fig.1). Since this time, inter-island 2014; Liu et al. 2014). Furthermore, hybridization or supply shipments by air and sea within the Cay- admixture between introduced and native taxa (e.g., mans—primarily from the capital and largest port on Fitzpatrick and Shaffer 2007) compromises the GrandCayman(196km2) to the much smaller genetic distinctiveness of taxa, including endemics, Cayman Brac (*38 km2) and Little Cayman unique phenotypes, and evolutionarily significant (\10 km2)—could have transported invasive and units (Moritz 1994). A previously undocumented native A. sagrei among this trio of islands. Indeed, in dimension of biological invasion occurs when inva- 2010, a single A. sagrei individual with a red dewlap sive populations from outside of their native range are was observed on Cayman Brac (T. Sanger, pers. reintroduced into native-range populations; either comm.) where only yellow dewlaps have been back into their original source population or, more observed previously, suggesting an introduction to generally, to any part of their native range. Guo (2005) Cayman Brac of invasive A. sagrei from Grand proposed the term ‘‘cryptic back-introduction’’ for this Cayman or native A. s. sagrei from Little Cayman. phenomenon, but to our knowledge it has never been In this study, we surveyed A. sagrei populations demonstrated. Here we explore whether this phe- across Cayman Brac looking for red-dewlapped nomenon is occurring in the brown anole lizard (A. lizards to determine whether invasive A. sagrei from sagrei) and consider the implications of this type of Grand Cayman have in fact invaded Cayman Brac. We invasion for native populations. also collected lizards on Grand Cayman and Little Anolis sagrei is a good natural colonizer, reaching Cayman to discriminate between these two potential many islands and mainland areas in the Caribbean by sources of red-dewlapped A. sagrei. For lizards from overwater dispersal (Williams 1969). During its up to all three islands, we quantified dewlap phenotypes 6.5 million year evolutionary history (based on using spectrophotometric methods, measured struc- coalescent dates from a molecular-clock calibrated tural habitat use and body size, and genotyped ten mtDNA gene tree provided by R.G. Reynolds, pers. nuclear microsatellite loci. For individuals with inter- comm.), this species colonized all of Cuba, most mediate multilocus genotypes or a genotype that did islands in the Bahamas, the Atlantic coast of Mexico not match their island, we sequenced mtDNA haplo- and Belize, and Swan Island (Schwartz and Hender- types (ND2) to test for nuclear-mitochondrial mis- son 1991). As long ago as 2.5 million years this matches. Using these data, we evaluated whether species also colonized Cayman Brac and Little invasive A. sagrei from Grand Cayman have been Cayman (R.G. Reynolds, pers. comm.), two small introduced to native populations on Cayman Brac, and 123 An incipient invasion of brown anole lizards (Anolis sagrei) Fig. 1 Map showing (A) portions of the native and non-native ranges of Anolis sagrei relevant to this study: a Arrows indicate routes of primary invasion from multiple native-range source populations in Cuba to the non-native range in Florida and a secondary invasion from non-native populations in south Florida to Grand Cayman; b the arrow indicates a cryptic back- introduction of invasive brown anoles from Grand Cayman into the native (B) range on Cayman Brac; and b, c circles show collection localities for genetic, ecological, morphological, and dewlap data on Grand (C) Cayman, Little Cayman, and Cayman Brac with site numbers corresponding to those listed in Table S1 if so, whether invasive lizards have interbred with (PX-2, Ocean Optics), calibrated regularly against a native lizards. white reflectance standard (Labsphere, Inc.). On live lizards, we measured reflectance at nine points distributed across the dewlap by pressing the dewlap Methods against a black background with the reflectance probe containing a black, 45°-angled tip used to prevent We sampled lizards in the Cayman Islands in January specular glare. The Ocean Optics software was set to a 2011, focusing the majority of our effort on Cayman boxcar width of five and an integration time of 10 ms. Brac due to the previous observation of a red- We averaged ten scans to generate spectra for each dewlapped A. sagrei there (Fig. 1; Table S1). On all point on the dewlap. three islands, for each undisturbed lizard encountered, We used the R-package pavo (Maia et al. 2013)to we measured perch height (cm) and perch diameter manipulate spectrophotometric data. Briefly, we used (cm), two key aspects of the structural habitat niche in the functions getspec to import our spectra within the anoles (Losos 2009). We also measured two aspects of 300–700 nm wavelength window, aggspec to generate body size, snout-vent length (SVL, mm) and mass (g), a mean spectrum for each individual, and procspec to for all lizards captured.
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