Figure 1. Native and non-native ranges of Anolis sagrei. Map from Kolbe et al. (2017).In this study, Kolbe and collaborators (2017) surveyed A. sagrei populations across Cayman Brac. First, they looked for red-dewlapped lizards to determine whether invasive A. sagrei from Grand Cayman have invaded Cayman Brac. Second, they collected brown anole lizards on Grand Cayman and Little Cayman to determine the source of red-dewlapped A. sagrei. For all lizards captured, they quantified dewlap phenotypes (i.e., reflectance spectra) using spectrophotometric methods, measured structural habitat use (i.e., perch height and diameter) and body size (i.e., snout-vent length (SVL) and mass), and genotyped ten nuclear microsatellite loci. For lizards with intermediate multilocus genotypes or with a genotype that did not match their island, they sequenced mitochondrial DNA (mtDNA) haplotypes (ND2) to test for nuclear-mitochondrial mismatches. Genomic data was combined with previously published microsatellite genotypes (Kolbe et al. 2008) and mtDNA (ND2) sequences for the Cayman Islands (Kolbe et al. 2004, 2007). With these data, they evaluated whether invasive A. sagrei from Grand Cayman have been introduced to native populations on Cayman Brac, and if so, whether invasive lizards have interbred with native lizards.

Under current trends of globalization, human activities impact the distribution of species by facilitating dispersal of propagules. Human-mediated dispersal prevents geographic distance from being a barrier to the introduction and movement of many species. These long-distance colonization events can gather evolutionary distinct lineages that might have been separated for millions of years (e.g., Kolbe et al. 2004). Moreover, dispersal events can potentially reintroduce individuals from an invasive population back into their native range; either back into their original source population or to any part of their native range. This previously undocumented dimension of biological invasion was termed cryptic back-introduction by Guo (2005).

Anolis sagrei is an excellent colonist, judging by its geographical distribution. This species has reached many islands and mainland areas in the Caribbean by overwater dispersal (Williams 1969). About 2.5 million years ago, A. sagrei naturally colonized Cayman Brac and Little Cayman. These populations subsequently differentiated into the yellow-dewlapped endemic subspecies A. sagrei luteosignifer on Cayman Brac and the red-dewlapped A. s. sagrei on Little Cayman (Schwartz and Henderson 1991); the dewlap (i.e., an extendible flap of skin attached to the throat) is used for mate attraction, male-male and interspecific competition, and predator deterrence (Losos 2009). However, this species failed to naturally colonize the third of the Cayman Islands, Grand Cayman. In the early 1980s, through human-mediated dispersal, a red-dewlapped form of A. sagrei established on Grand Cayman. These populations resulted from the introduction of genetically admixed lizards from non-native populations in south Florida (Minton and Minton 1984; Kolbe et al. 2004, 2008; Figure 1). Since then, inter-island supply shipments by air and sea within the Caymans could have transported invasive and native brown anole lizards among the three islands. Kolbe et al. (2017) explored whether cryptic back-introduction is occurring in brown anole (A. sagrei) lizards and the implications of this type of invasion for native populations.

Figure 2. Results of PCA for dewlap reflectance (Kolbe et al. 2017).

Kolbe et al. (2017) found no differences among islands in structural habitat use. They conducted a principal component analysis (PCA) for dewlap reflectance data using the average wavelength of each lizard. PCA results show that there is strong differentiation in dewlap reflectance between yellow-dewlapped lizards on Cayman Brac and the red-dewlapped lizards on Little Cayman and Grand Cayman (Figure 2), which supports their field observations of red-dewlapped lizards occurring on Cayman Brac (Figure 3B). This suggests the introduction of brown anole lizards to Cayman Brac from either of the two other Cayman Islands.

Figure 3. Examples of Anolis sagrei dewlaps from the Cayman Islands (Kolbe et al. 2017).

Furthermore, this study reports strong population-genetic structure among the three Cayman Islands and evidence for non-equilibrium. They identified intermediate multilocus genotypes between Grand Cayman and Cayman Brac (Figure 4). Also, the authors found an intermediate microsatellite genotype in one individual from Cayman Brac. This lizard had a red dewlap and a mtDNA haplotype from Grand Cayman. This mismatch among genetic and phenotypic data suggests that A. sagrei lizards (with different colored dewlaps) from Grand Cayman and Cayman Brac are interbreeding.

Figure 4. Results of a PCoA using multilocus genotypes from ten microsatellite loci (Kolbe et al. 2017).

This study reports the first evidence of cryptic back-introduction; however the frequency with which this phenomenon occurs is still unknown. By studying cryptic back-introductions we can eventually understand how lineages change though a brief period of isolation from its native range and determine if these are incompatible when brought together again. Likewise, future studies should address how phenotypic variation affects ecological interactions with native species and its consequences.

Article:

Kolbe, J. J., J. E. Wegener, Y. E. Stuart, U. Milstead, K. E. Boronow, A. S. Harrison, and J. B. Losos. 2017. An Incipient Invasion of Brown Anole Lizards (Anolis sagrei) Into Their Own Native Range in the Cayman Islands: A Case of Cryptic Back-introduction. Biological Invasions 19:1989–1998.

Cited Literature:

Guo, Q. 2005. Possible cryptic invasion through “back introduction”?

Kolbe, J. J., R. E. Glor, L. R. Schettino, A. C. Lara, A. Larson, and J. B. Losos. 2004. Genetic variation increases during biological invasion by a Cuban lizard. Nature 431:177–181.

Kolbe, J. J., A. Larson, and J. B. Losos. 2007. Differential admixture shapes morphological variation among invasive populations of the lizard Anolis sagrei. Molecular Ecology 16:1579–1591.

Kolbe, J. J., A. Larson, J. B. Losos, and K. de Queiroz. 2008. Admixture determines genetic diversity and population differentiation in the biological invasion of a lizard species. Biology letters 4:434–437.

Losos, J. B. 2009. Lizards in an Evolutionary Tree: Ecology and Adaptive Radiation of anoles. University of California Press.

Minton SA, Minton MR (1984) Anolis sagrei (brown anole). Herpetol Rev 15:77

Schwartz A, Henderson RW (1991) Amphibians and reptiles of the West Indies: descriptions, distributions, and natural history. University of Florida Press, Gainesville

Williams, E. E. 1969. The ecology of colonization as seen in the zoogeography of anoline lizards on small islands.

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