Historical Perspective On Anole Genera

Anole taxonomists: Richard Etheridge, Jay Savage, Ernest Williams, S. Blair Hedges, Craig Guyer, Steve Poe

Anolis has been recognized as an extraordinarily large genus for decades, but Nicholson et al. (2012) are not the first to propose recognition of multiple anole genera. Indeed, all of the generic epithets used in Nicholson et al.’s new classification were coined in 1934 or earlier and most are from the early 19th century. This early proliferation of generic epithets resulted primarily from the fact that a comprehensive systematic treatment of anoles did not appear until the mid-20th century. My purpose here is to review the history of generic level anole classification in the years following Richard Etheridge’s pioneering PhD thesis of 1959/60. I believe that this historical perspective provides necessary context for evaluation of Nicholson et al.’s proposed revisions, and helps explain why the genera in their revised classification appear so rarely in the literature relative to Anolis (see Mahler’s recent post on the topic of genus name usage).

To briefly summarize the history of anole genera, the vast majority of work published over the past half century has formally assigned all, or nearly all, anole species to Anolis. The only noteworthy exceptions to this include (1) assignment of a small number of morphologically unusual species from the mainland, Cuba, or Hispaniola to Phenacosaurus, Chamaelinorops or Chamaeleolis into the 1990s and (2) assignment of species belonging to Etheridge’s β section of Anolis to Norops by some anole biologists working primarily in Central America during the 1990s through the 2000s.

Etheridge’s dissertation, which was completed in 1959 but not available until 1960.

In 1959, Richard Etheridge, a PhD student with Norman Hartweg at the University of Michigan, submitted a thesis that relied on remarkably thorough analyses of skeletal morphology to revise anole classification. At the beginning of this study, Etheridge recognized Anolis as a diverse genus containing over 200 species, but also identified ten other anole genera that contained only one or a few species: Chamaeleolis, Phenacosaurus, Chamaelinorops, Tropidodactylus, Audantia, Mariguana, Diaphoranolis, Xiphocercus, Deiroptyx, and Norops. Etheridge found the first four genera listed above to be “so unusual” morphologically that they warrant continued recognition, but the rest were synonomized with Anolis because his morphological analyses found them “to be not at all separable from Anolis, or to be based on characters so trivial that they are here considered as identical with Anolis.”

Etheridge left the large genus Anolis intact in spite of the fact that, at the beginning of his study, he “thought it very likely that the great number of species in the genus Anolis might be dividied into several groups, and that each of these might reasonably be accorded generic status.” His reason for leaving Anolis intact was that “the relationships of the various species of Anolis have proven to be far too complex to be treated in so simple a manner as the proposal of formal generic groupings.” Rather than naming new genera, Etheridge informally characterized sets of species at “several different hierarchical positions between the genus and species” as “groups,” “complexes,” “sections,” or “series.” The aspect of Etheridge’s classification that drew the most attention was his division of Anolis into α and β sections distinguished primarily on the basis of basis of a striking difference in the morphology of tail vertebrae (see figure above from Etheridge’s disseration).

Savage’s 1973 pamphlet that applies either Anolis or Norops to Costa Rican anole species.

Most authors in the 1960s and 70s followed Etheridge’s proposed taxonomy by recognizing Anolis as a large genus containing most anole species. However, Jay Savage, who was then at USC, rejected Etheridge’s proposed taxonomy in a pamphlet containing a preliminary handlist of the herpetofauna of Costa Rica that was prepared for the benefit of colleagues attending the 53rd annual meeting of the American Society of Ichthyologists and Herpetologists in San Jose, Costa Rica. In this pamphlet, Savage used Norops for the species in Etheridge’s β section and Anolis for the species in Etheridge’s α section. As far as I know, this pamphlet marks the beginning of Savage’s long-standing advocacy for breaking Anolis (sensu Etheridge) into multiple genera, and for his use of Norops to describe Etheridge’s β section in particular.

In 1976, Ernest Williams, who was then professor and curator in the Museum of Comparative Zoology at Harvard, produced two reports that together provided a new classification of anoles found everywhere except Central America. Williams (1976a, b) recognized three genera, two that were “old, species-poor and obviously relict” (Chamaelinorops and Chamaeleolis) and one that was “species-rich beyond ordinary imagining” (Anolis). The two species-poor genera were found in the West Indies and included morphological unusual species endemic to Hispaniola (Chamaelinorops barbouri) and Cuba (Chamaeleolis). Following Etheridge, Williams recognized diversity within Anolis by diagnosing a large number of series and species groups.

Shortly after the publication of Williams’s classification, Jay Savage and one of his PhD students at USC (James Talbot) formalized the taxonomic practice that Savage had earlier applied without explanation in the 1973 handlist by proposing recognition of Etheridge’s β section as Norops and Etheridge’s α section as Anolis (Savage and Talbot 1978). Savage and Talbot (1978) noted that everything since Etheridge’s thesis had supported the α/β distinction, and called attention to the fact that the characters investigated by Etheridge “are usually family specific elsewhere among lizards and always generically consistent elsewhere in the family Iguanidae.” Nevertheless, Savage and Talbot’s proposed generic revision was largely disregarded by other anole systematists, at least in part because molecular studies conducted in the early 1980s confirmed earlier suspicions that the alpha section (=Anolis sensu Savage and Talbot 1978) would be rendered paraphyletic by the beta section (=Norops sensu Savage and Talbot 1978) (Wyles and Gorman 1980, Shochat and Dessauer 1981).

Writing with Talbot, Savage presaged subsequent efforts to divide anoles into additional genera when he suggested that “these two speciose genera [Anolis and Norops] may be further sub-divided into smaller genera based on suites of diverse characters as the knowledge of anole evolution progresses, as suggested by Williams (1963).” Ten years later, and after moving to the University of Miami, Savage followed through on this suggestion by joining with another of his PhD students (Craig Guyer) to propose a comprehensive new classification for anoles based on reanalyses of existing osteological, karyotypic, and albumin immunological data (Guyer and Savage 1986, Savage and Guyer 1989). This classification divided anoles into eight genera, including the three morphologically unusual and putatively “primitive” genera recognized previously by Etheridge and Williams (Chamaeleolis, Chamaelinorops, and Phenacosaurus), as well as five new genera that included the species that Etheridge and Williams had assigned to Anolis. Three of the newly erected genera consisted of species endemic to the West Indies (Ctenonotus, Semiurus [which was later changed to Xiphosurus by Savage and Guyer 1991 due to priority issues], and Anolis)* while two of the newly erected genera included species found both in the West Indies and the mainland (Dactyloa and Norops).

Guyer and Savage’s new arrangement was criticized both by Williams (1989) and Cannatella and de Queiroz (1989) for a number of reasons, most importantly because some of the newly erected genera were not demonstrably monophyletic and because formal fragmentation of Anolis into new genera was deemed likely to generate more confusion than it would clarity.

Guyer and Savage (1992) defended their proposed taxonomic arrangement against all of these criticisms. In the 1990s, some prominent anole biologists working with Central and South American anoles – including Jonathan Campbell, James McCranie, Gunther Köhler, and Laurie Vitt – followed Guyer and Savage by recognizing Norops, and, less frequently Dactyloa. Other mainland workers and essentially everyone working on West Indian anoles, however, followed Williams (1989) and Cannatella and de Queiroz (1989) in dismissing Guyer and Savage’s proposed generic revision. As a result, the names applied to West Indian taxa – Ctenonotus, Semiurus/Xiphosurus and Anolis (sensu Guyer and Savage 1986) – almost never appear in the literature; with some of the only exceptions being a paper on West Indian biogeography published by Guyer and another Savage student (Brian Crother) and numerous field-guides and checklists for the mainland that include species introduced from the West Indies (e.g., Ctenonotus cristatellus in Köhler’s Reptiles of Central America and Leenders’s guide to the amphibians and reptiles of Costa Rica).

This break in the taxonomic practices of anole researchers working on the mainland versus those working in the West Indies has two fairly obvious explanations. First, the mainland anole fauna is far less phylogenetically complicated than that of the West Indian species; the two genera found on the mainland that were diagnosed by Guyer and Savage (Norops and Dactyloa) have tended to form monophyletic groups in subsequent phylogenetic analyses, while three of the five genera found in the West Indies have not formed monophyletic groups in one or more subsequent phylogenetic analyses. Second, Savage and Guyer were themselves widely respected authorities on the Central American herpetofauna. Indeed, Savage and his students have been the primary authorities on the Costa Rican herpetofauna for decades, and by the late 1980s Savage had already published numerous handlists and species keys recognizing Norops that were widely used by biologists working in Costa Rica (including the 1973 pamphlet that initiated formal use of Norops).

In 1991, Burnell and Hedges published a new classification of West Indian anoles based on phylogenetic trees generated from slow-evolving protein loci sampled from 49 species. This study rejected Guyer and Savage’s (1986) formal generic revision and followed Etheridge and Williams in recognizing diversity within a species rich Anolis (sensu Etheridge and Williams) using informal series and species groups.

Although Burnell and Hedges considered the enigmatic Chamaelinorops as a likely outgroup to Anolis, they were among the last to do so. Just two years later, Hass, Hedges, and Maxson (1993) used additional data to show that both Chamaelinorops and Chamaeleolis “are recent derivatives within the genus Anolis.” As a result, two of the non-Anolis anole genera that were recognized by nearly all anole biologists from Etheridge’s time through the 1980s were synomized with Anolis. Phenacosaurus was the last of the non-Anolis anole genera recognized by Etheridge and most others to fall into the synonmy of Anolis, when Poe (1998) showed conclusively that Phenacosaurus was nested within Anolis.

Shortly after all of the “primitive” and “enigmatic” genera recognized by most anole biologists prior to the 1990s where synonomized with Anolis, the first reasonably comprehensive phylogenetic studies of anoles based on mitochondrial DNA began to emerge in the late 1990s (Losos et al. 1998, Jackman et al. 1999). Although publication of these studies was not accompanied by comprehensive new anole classifications, the resulting trees tended to be much better supported than those produced by previous datasets and tended to support monophyly of three of the new genera proposed by Guyer and Savage (Norops, Dactyloa, Xiphosurus) while rejecting monophyly of the other two (Anolis, Ctenonotus). Moreover, these studies confirmed that the putatively “primitive” clades diagnosed previously as Chamaelinorops, Chamaeleolis, and Phenacosaurus were actually nested within a paraphyletic Anolis.

In 2004, Poe, a former undergraduate student of Ernest Williams’s at Harvard, published another landmark paper in history of anole systematics. This paper resulted from Poe’s PhD thesis conducted under David Cannatella and David Hillis at UT Austin and included a remarkable new morphological dataset and detailed phylogenetic analyses of this new morphological data along with previously published mitochondrial DNA sequence data. Poe (2004) rejected Guyer and Savage’s (1986) formal generic revision, in part because his own analyses rejected monophyly of some of their proposed genera. Poe followed previous anole systematists such as Etheridge, Williams, and Hedges by recognizing diversity within a species rich Anolis using informal series and species groups. Poe’s paper was the last comprehensive treatment of anole classification prior to the publication last month of Nicholson et al.’s new monograph. Nicholson et al.’s proposed classification, which will we will be discussing in detail throughout the coming week, is the third proposed taxonomic revision published by Savage and his students that divides Anolis into a number of smaller genera.

* The only exception to West Indian endemicity in these clades is the North American species A. carolinensis, which appears to be a relatively recent immigrant from Cuba.

References

Burnell, K. L., and S. B. Hedges. 1990. Relationships of West Indian Anolis (Sauria: Iguanidae): an approach using slow-evolving protein loci. Caribbean Journal of Science 26:7–30. [pdf link]

Cannatella, D. C., and K. de Queiroz. 1989. Phylogenetic systematics of the anoles: is a new taxonomy warranted? Systematic Zoology 38:57–69. [jstor link]

Etheridge, R. 1960, September 14. The relationships of the Anoles (Reptilia; Sauria; Iguanidae); an interpretation based on skeletal morphology. University of Michigan, Ann Arbor, Ann Arbor, Michigan.

Guyer, C., and J. M. Savage. 1986. Cladistic relationships among anoles (Sauria: Iguanidae). Systematic Biology 35:509–531. [jstor link]

Guyer, C., and J. M. Savage. 1992. Anole systematics revisited. Systematic Biology 41:89–110. [jstor link]

Hass, C. A., S. B. Hedges, and L. R. Maxson. 1993. Molecular insights into the relationships and biogeography of West Indian anoline lizards. Biochemical Systematics and Ecology 21:97–114. [doi link]

Jackman, T. R., A. Larson, K. de Queiroz, and J. B. Losos. 1999. Phylogenetic relationships and tempo of early diversification in Anolis lizards. Systematic Biology 48:254–285. [doi link]

Losos, J. B., T. R. Jackman, A. Larson, K. de Queiroz, and L. Rodriguez-Schettino. 1998. Contingency and determinism in replicated adaptive radiations of island lizards. Science 279:2115–2118. [doi link]

Nicholson, K. E., B. I. Crother, C. Guyer, and J. M. Savage. 2012. It is time for a new classification of anoles (Squamata: Dactyloidae). Zootaxa:1–108.

Poe, S. 1998. Skull characters and the cladistic relationships of the Hispaniolan dwarf twig Anolis. Herpetological Monographs:192–236. [jstor link]

Poe, S. 2004. Phylogeny of anoles. Herpetological Monographs:37–89. [jstor link]

Savage, J. M., and J. J. Talbot. 1978. The giant anoline lizards of Costa Rica and western Panama. Copeia:480–492. [jstor link]

Savage, J. M., and C. Guyer. 1989. Infrageneric classification and species composition of the anole genera, Anolis, Ctenonotus, Dactyloa, Norops and Semiurus (Sauria: Iguanidae). Amphibia-Reptilia 10:105–115.

Savage, J. M., and C. Guyer. 1991. Nomenclatural notes on anoles (Sauria: Polychridae): stability over priority. Journal of Herpetology 25:365–366.

Shochat, D., and H. C. Dessauer. 1981. Comparative immunological study of albumins of Anolis lizards of the Caribbean islands. Comparative Biochemistry and Physiology Part A: Physiology 68:67–73.

Williams, E. E. 1976a. West Indian Anoles: a taxonomic and evolutionary summary. I. Introduction and a species list. Breviora 440:1–21.

Williams, E. E. 1976b. South American anoles: the species groups. Papéis Avulsos de Zoologia 29:259–268.

Williams, E. E. 1989. A critique of Guyer and Savage (1986): cladistic relationships among anoles (Sauria: Iguanidae): are teh data available to reclassify the anoles? Pages 433–478 in C. A. Woods, editor. Biogeography of the West Indies. Sandhill Crane Press, Gainesville, FL.

Wyles, J. S., and G. C. Gorman. 1980. The classification of Anolis: conflict between genetic and osteological interpretation as exemplified by Anolis cybotes. Journal of Herpetology 14:149–153. [jstor link]