An illustration from Gosse (1851) depicting Jamaica’s crown-giant, Anolis garmani (note that Gosse used the old name, “Dactyloa Edwardsii”), adjacent to a West Indian boid (Chilabothrus).
Jamaica’s six endemic Anolis species–A. garmani, A. reconditus, A. valencienni, A. lineatopus, A. grahami, and A. opalinus–have long captured the fascination of Caribbean naturalists. And how could they not? Although only six, these lizards are among the Caribbean’s most eye-grabbing. Take it from Phillip Henry Gosse, who recounted his experience catching one of these six species using a twine lasso in A Naturalist’s Sojourn in Jamaica (1851):
“The mode in which I formed an acquaintance with the species may be worthy of being related. One day in February, having ascended the ridge with a companion, my attention was arrested by a Lizard about a foot long, and of a lively green colour, on the trunk of a small tree, head downward, intently watching our motions as we stood near. My young friend suggested the possibility of capturing it by slipping a noose over its head, while its attention was engaged by whistling. I laughingly proceeded to try the spell; and having made a noose of small twine, which I tied to the end of a switch, I gently walked towards him, whistling a lively tune. To my astonishment he allowed me to slip the noose over his head, merely glancing his bright eye at the string as it passed. I jerked the switch; the music ceased; and the green-coated forester was sprawling in the air, dangling, greatly to his annoyance, at the end of my string. He was very savage, biting at every thing near; presently his colour began to change from green to blackish, till it was of an uniform bluish black with darker bands on the body, and a brownish black on the tail: the only trace of green.”
Since Gosse’s work on West Indian reptiles (including formal designation of the Jamaican anole radiation as Placopsis), much has changed in our understanding of Jamaica’s Anolis diversity and evolution. In 2002, Todd Jackman and colleagues published a study aiming to estimate the phylogenetic relationships among Jamaica’s anoles.
The authors found support for the following topology (Jackman et al. 2002; Fig. 7): A. lineaotopus and A. reconditus form a clade that is sister to the remaining Jamaican anoles, followed by A. valencienni, A. garmani, and, ultimately, A. grahami + A. opalinus. Jackman et al. would continue in the same paper to discuss phylogeography and intraspecific divergences. Notably, a single A. opalinus from Hardwar Gap (Blue Mountains) appeared to be more closely allied to A. valencienni than to other sampled A. opalinus individuals. This diverse array of mitochondrial haplotypes recovered from A. opalinus then raises the question, does the history of Anolis on Jamaica involve hybridization, or is it merely a result of incomplete lineage sorting we may expect from a rapid adaptive radiation?
Nearly twenty years went by without an answer. Was the phylogenetic hypothesis posited by Jackman et al. correct? What’s going on with A. opalinus? Separately, in the two decades since the work by Jackman and colleagues, a revolution has occurred in phylogenetic biology. In the study of phylogeny, if introgression (e.g., ancient mitochondrial capture as a result of hybridization) has played a role in shaping the evolutionary history of the relevant group, it’s important that we test if such events have occurred, and subsequently be able to disentangle and ultimately account for them in our phylogenetic estimations. Failure to do so can lead to misleading topologies, inaccurate reconstructions of evolutionary histories and parameter estimates, as well as shortcomings in accurately describing and recognizing biodiversity.
Luckily, resolution to this issue has been afforded by several folks (Claudia Solís-Lemus and Cécile Ané, to name just two) who have developed statistical methods to detect and account for both incomplete lineage sorting (ILS) and reticulate patterns of evolution (introgression). So, how does this relate to those oh-so-cool Jamaican anoles? This is where Myers et al. (2021) come in.
In a new study in the Spotlight section of Systematic Biology, Myers and colleagues re-open the investigation into Jamaican Anolis phylogeny using the aforementioned suite of novel methods. For those in attendance at the Joint Meeting of Herpetologists and Ichthyologists in 2018, the early stages of this work were presented by students conducting research at the American Museum of Natural History, previously featured on Anole Annals. Using genotyping-by-sequencing (an approach that has been applied elsewhere in Anolis research), the authors generate swaths of SNP data from the nuclear genome. To be exact, the total dataset comprised 257,317 base pairs (just over 2,900 loci). Restriction-site-associated approaches (i.e., RAD-Seq) to sequencing DNA have made it feasible to capture large, representative samples of the nuclear genome at low cost.
Armed with data from both the nuclear and mitochondrial genomes, Myers et al. (2021) found dramatically different relationships and evolutionary histories among species between the two sources. Figure 3 demonstrates this disparity well, and further hammers home the general dangers of violating model assumptions in phylogenetic inference (in this case, the multi-species coalescent [MSC] model, which assumes a lack of gene flow among sampled taxa).
First, when using solely the mtDNA data in a MSC framework, the authors find A. opalinus from the Blue Mountains to be polyphyletic, a result concordant with the inference of Jackman et al. (2002). Specifically, one A. opalinus lineage (Blue Mountains) is sister to A. valencienni, whereas the other A. opalinus lineage is sister to A. grahami. Notably, the time calibrated mtDNA gene-tree suggests the two A. opalinus mtDNA genomes are more than 30 million years divergent!
The authors then infer a species tree using the GBS data in an MSC framework (one that assumes gene-tree species-tree discordance can be attributed to incomplete lineage sorting and accounts for such). With this tree, the two A. opalinus lineages form a clade sister to A. grahami and A. garmani. Finally, with SnaQ (a modeling program developed by Solís-Lemus and colleagues to infer reticulation events across a tree), the authors recovered an identical topology to the nuclear DNA based species-tree, but with high support for a single introgression event (and hence, reticulate evolution) between A. opalinus and A. grahami. Using simulations, Myers and colleagues provide evidence against ILS as the causative agent for gene-tree species-tree discordance, favoring hybridization as the culprit.
I won’t spoil the Discussion, but much of Jamaican Anolis evolution remains open-ended (including the role of adaptive introgression in shaping Anolis communities). It’s probably safe to say Gosse wasn’t pondering the possibility of adaptive introgression in shaping Jamaican Anolis phylogeny. However, resolution of the outstanding questions identified by Myers et al. (2021) will come primarily through Gosse’s philosophy–getting out in the field, catching lizards, and getting a more-fine scale, phylogeographic picture of the variation over space and time in Jamaican Anolis.
I thank Ed Myers and Kevin de Queiroz for feedback on this blog post.
Literature Cited:
Jackman, T. R., Irschick, D. J., De Queiroz, K., Losos, J. B., & Larson, A. 2002. Molecular phylogenetic perspective on evolution of lizards of the Anolis grahami series. Journal of Experimental Zoology 294(1) 1-16.
New literature alert!
Interspecific Gene Flow and Mitochondrial Genome Capture During the Radiation of Jamaican Anolis Lizards (Squamata; Iguanidae)
In Systematic Biology
Myers, Mulcahy, Falk, Johnson, Carbi, de Queiroz
Gene flow and reticulation are increasingly recognized as important processes in the diversification of many taxonomic groups. With the increasing ease of collecting genomic data and the development of multispecies coalescent network approaches, such reticulations can be accounted for when inferring phylogeny and diversification. Caribbean Anolis lizards are a classic example of an adaptive radiation in which species have independently radiated on the islands of the Greater Antilles into the same ecomorph classes. Within the Jamaican radiation at least one species, A. opalinus, has been documented to be polyphyletic in its mitochondrial DNA, which could be the result of an ancient reticulation event or incomplete lineage sorting. Here we generate mtDNA and genotyping-by-sequencing (GBS) data and implement gene-tree, species-tree, and multispecies coalescent network methods to infer the diversification of this group. Our mtDNA gene-tree recovers the same relationships previously inferred for this group, which is strikingly different from the species-tree inferred from our GBS data. Posterior predictive simulations suggest that our genomic data violate commonly adopted assumptions of the multispecies coalescent model, so we use network approaches to infer phylogenetic relationships. The inferred network topology contains a reticulation event but does not explain the mtDNA polyphyly observed in this group, however coalescent simulations suggest that the observed mtDNA topology is likely the result of past introgression. How common a signature of gene flow and reticulation is across the radiation of Anolis is unknown; however, the reticulation events that we demonstrate here may have allowed for adaptive evolution, as has been suggested in other, more recent adaptive radiations.
Photo: Steve Maldonado Silvestrini, 
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