Introduction

“…it appears that the true history of the colonization of the land, now Bermuda, is lost forever in oblivion” [1]

Studies of island biodiversity have focused largely on adaptive radiations associated with neoendemism (i.e., “cradles” of diversity) [2]–[4]. There are myriad factors that promote spectacular biodiversity on islands, but the factors that contribute to neoendemism ultimately derive from the fact that the islands formed de novo with no connection to a larger landmass and thus have abundant “empty” ecological niche space. However, the isolation that defines islands can also preserve genetic diversity of relict lineages, a pattern known as paleoendemism [3], [5]. The most prominent example of this phenomenon among vertebrates is the tuatara (Sphenodon) that represents a clade of reptiles once widespread, but now restricted to two remaining species found only on the offshore islands of New Zealand. Moreover, given numerous threats such as climate change, introduced species, and habitat destruction, insular fauna are subject to increased risk of extinction [6]. This vulnerability is of particular concern for paleoendemics, as these taxa represent a disproportionately high amount of phylogenetic diversity [7]–[9].

The islands of Bermuda (32.33°N, 64.75°W) are an isolated, 54 km² archipelago (referred to as “island”, hereafter) approximately 1000 km east of the United States (Fig. 1a). The island is currently home to a single endemic terrestrial vertebrate, the scincid lizard Plestiodon longirostris (formerly Eumeces longirostris [10], [11]), although several other terrestrial vertebrates, including a tortoise (Hesperotestudo) and multiple species of birds, inhabited the island until from the Middle to Late Pleistocene [12]–[19]. Plestiodon longriostris is currently considered critically endangered [20] and faces continuing threats of extinction through human-caused habitat loss, competition with and predation from introduced species, and entrapment in discarded bottles [21]. Once abundant [22], [23], the species' range has dwindled to several small sub-populations, the largest of which occurs on Southampton Island and contains only an estimated 400 individuals [21]. Preliminary microsatellite analysis indicates that the current genetic diversity of P. longirostris is low [24].

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Figure 1. The location of Bermuda, phylogeny of Plestodon, and molecular estimates of divergence times.

a., Map showing the location of Bermuda relative to North America. b., Phylogeny of the genus Plestiodon (outgroups not shown; see Brandley et al, 2010). Branch lengths are in units of time and represent the means of the posterior distribution. Numbers above or below the nodes indicate posterior probabilities. Triangles indicate groups for which multiple species were sampled, but are not shown. Taxa in blue are those that inhabit eastern North America. Green bars indicate the 95% credible interval for estimated divergence dates for that node. c., Posterior probability distribution of the age of the divergence between Plestiodon longirostris and its sister lineage. Areas shaded in red are values that exceed the 95% credible interval.

https://doi.org/10.1371/journal.pone.0011375.g001

Pre-plate tectonics biogeographic hypotheses assumed that P. longirostris was a relict of an ancient lineage that became isolated on Bermuda after the closing of a land bridge [1]. This “relict” hypothesis was also influenced by the species' unique morphological characteristics (including an elongated snout). However, recent geologic studies have demonstrated that, although part of an ancient, volcanic sea-mount, most of the exposed, terrestrially habitable portion of Bermuda has never been connected to a larger landmass and instead consists of limestone deposited in the Pleistocene [25]–[28], the maximum age of which is no more than two million years [29]. Moreover, all known Bermudan vertebrate fossils are limited to sediments from the latter half of the Pleistocene [13]–[19]. A more reasonable alternative hypothesis is that the species is quite young, at most as old as the maximum age of Bermuda (1–2 million years), and is a descendent of one of the several species of Plestiodon inhabiting the eastern United States that dispersed over water to Bermuda following the emergence of the island. Another reptile (indeed, the only other potentially native reptile), the diamondback terrapin (Malaclemys terrapin), is a likely very recent immigrant that descended from populations of the same species that currently inhabit the eastern United States [30], [31].

To evaluate the evolutionary history of this unique skink, and specifically to test the “relict” and “recent immigrant” hypotheses, we conducted Bayesian relaxed molecular clock divergence dating analyses of an extensive, multi-locus DNA data set including all Plestiodon species from the eastern United States and the Bermudan P. longirostris. We demonstrate that the oceanic island of Bermuda, despite its young age (no more than two million years) and history of extreme changes in available habitat, harbors the last representative of one of the earliest North American lineages of Plestiodon that diverged ∼16 million years ago.

Results and Discussion

The results of the phylogenetic analysis (pruned to show relevant taxa only; Fig. 1b) show that the lineage that includes modern P. longirostris does not descend from any of the extant Plestiodon lineages that inhabit eastern North America. In fact, Bayesian divergence dating analyses using a relaxed molecular clock indicate that it is one of the earliest diverging lineages of the entire North American clade (Figs. 1b,c). Furthermore, this divergence occurred ∼16 million years ago (Ma) (95% credible interval = 11.5 to 19.8 Ma), well before any modern species, and the lineage contains no extant representative other than P. longirostris. We are therefore left with the remarkable conclusion that a two million-year-old island contains the sole survivor of an ancient lineage that predates the existence of Bermuda by well over 10 million years.

Although no fossils of the P. longirostris lineage are known from mainland North America [1], the phylogenetic and divergence date data clearly indicate that ancestors once existed on the mainland. However, P. longirostris is present in Bermudan fossil beds dated to approximately 400,000 years ago. Given the young age of Bermuda, these results support the hypothesis that within the past 400,000 to two million years, individuals from the North American mainland P. longirostris lineage dispersed to a presumably recently emerged Bermuda 1000 km offshore, yet subsequently became extinct on the mainland. Although we can only speculate how these colonizing individuals dispersed over water, we note that both hurricanes and ocean currents are known to transport living lizards and debris to and from islands [32]–[33], and that the powerful Gulf Stream ocean current runs along eastern North America to the mid-Atlantic Ocean [see 31].

Thus, despite its young age, the island preserves the last representative of one of the oldest lineages of mainland North American Plestiodon – it is essentially an evolutionary “life raft”. This “life raft” role is remarkable considering that extreme fluctuations in sea level during the Pleistocene have intermittently decreased the available terrestrial habitat on Bermuda by orders of magnitude [18]. This extreme contraction in habitat was the likely cause of the extinction of several endemic birds [13]–[19]. Bermuda's only other native reptile, Malaclemys terrapin, only colonized the island in the past 3000 to 400 years from populations that currently inhabit the Eastern United States [30].

These results are extremely unlikely to be the result of error in divergence date estimates or phylogenetic uncertainty. One advantage of Bayesian methods of divergence dating is their ability to incorporate error in both the calibration age constraint and phylogeny, and to infer posterior probability distributions of estimated ages. The 95% credible interval of the date of divergence between P. longirostris and other North American Plestiodon species ranges from 11.5 to 19.8 Ma and excludes the earliest date that Bermuda may have emerged (2 Ma). Although the relationship between P. longirostris and its sister lineage is not well supported (posterior probability<0.95), this species is nonetheless excluded from any other younger clades with strong statistical support (Fig. 1b). In other words, the lineage cannot be any younger than the other major clades that all predate the emergence of Bermuda. Furthermore, if this lack of resolution represents a rapid radiation at the base of the North American Plestiodon phylogeny, then the age of the P. longirostris lineage is even older (∼13–21 Ma; Fig. 1b). Finally, extensive analyses of this data set have demonstrated that the use of models that account for rate heterogeneity among subsets of the DNA dramatically improve divergence date estimates and help mitigate potential problems inherent in using distantly related age calibrations [34].

We also note that the history of P. longirostris somewhat parallels that of the extinct Bermudan turtle, Hesperotestudo bermudae. Fossil evidence indicates this species became extinct on Bermuda 300,000 years ago, yet was the last representative of a genus of tortoise that inhabited North America from the Oligocene to Pleistocene [13], [18]. With the caveat that more recent fossils of North American Hesperotestudo may yet to be discovered, these data currently suggest that Bermuda also served as an evolutionary life raft for this genus after extinction on the mainland.

Although we certainly do not discount the profoundly important role of islands in generating biodiversity, our results highlight the frequently overlooked role of islands in preserving diversity (acting as evolutionary “museums”). This role is of particular importance given that preservation of phylogenetic diversity has been an increasingly important goal of conservation biology as the extinction of “old” species would result in a greater loss of genetic diversity than that of a “young” species with close phylogenetic relatives [7]–[9]. Therefore, because the Bermuda skink, Plestiodon longirostris, represents the sole representative of one of the earliest diverging lineages among North American Plestiodon, efforts to preserve this species are also preserving ∼12 to 20 millions of years of unique evolutionary history at the risk of extinction.

Materials and Methods

Supporting Information

Acknowledgments

We thank J. Davenport, A. Dornburg, J. McGuire, A. Seago, and one anonymous reviewer for advice and/or comments on the manuscript; J. Aguilar, K. Ashton, J. Campbell, S. Daniels, U. García, L. Kitson, J. Lazell, I. López, R. Macey, A. Mendoza, M. Mociño, R. Murphy, E. Pérez, T. Reeder, J. Richmond, CAS, FMNH, KUZ, LSUMZ, MVZ, UMMZ, and YPM for providing tissue samples; and J. Ichikawa, I. Katsube, A. Mendoza Hernández, E. Pérez Ramos, A. Seago, and Y. Yamamoto for fieldwork assistance.