Anole Annals

Figure 3 from Helmus and Ives (2012)

For 50 years, scientists have been cataloguing the relationship between area of islands or other patches of habitat and the number of species they contain. In general, the bigger the area, the greater the number of species. In recent years with the rise of interest in incorporating a phylogenetic perspective to all manner of questions, some have wondered how the phylogenetic variety (the degree of relatedness among species) changes with area. In an important new paper, Helmus and Ives take a theoretical perspective to understand what the expectation is for the relationship between phylogenetic diversity and area. Most excitingly, they illustrate their method using data from anoles on Caribbean islands.

Here’s how they describe what they’ve found: “While there was a strong relationship between Anolis species richness and Caribbean island bank area (Fig.3A; Losos 1996, Losos and Schluter 2000), we found no overall relationship between Anolis phylogenetic diversity and island bank area (Fig. 3B) …The greatest variation in phylogenetic diversity was associated with the overall level of in situ speciation … [T]here is a strong PDAR for the seven Caribbean island banks with at least one in situ speciation event (Fig. 4A). The estimated phylogenetic diversity values of these seven banks are dominated by in situ speciation as opposed to among-island allopatric events (Cuba had 2, 47, 49 colonizations, in situ events, species richness, respectively; Hispaniola had 4, 33, 37; Puerto Rico had 3, 11, 14; Jamaica had 1, 5, 6; Guadeloupe had 1, 3, 4; Grenada had 1, 1, 2; and St. Vincent had 1, 1, 2). The strong Anolis SAR causes a strong positive PDAR for these banks because species richness and the number of in situ speciation events positively correlate (Figs. 3A and 4B). If island assemblages were only derived from in situ speciation, then, according to the neutral macroevolutionary model we used, phylogenetic diversity is expected to positively increase, and then plateau with the number of in situ speciation events (Fig. 4C), which is the same relationship we found for the seven island banks (Fig. 4B). On at least the four Greater Antilles islands, island area sets a limit to the number of Anolis species that can arise via in situ speciation (Rabosky and Glor 2010). Thus, when there are no external colonizations that add large amounts of external evolutionary history to island assemblages, positive PDARs are expected.

It is the balance of ancestral colonizations to in situ speciation, therefore, that affects regional phylogenetic diversity. This balance is thought to be determined by a race between colonists, where initial colonist species will diversify if another colonist species does not arrive and establish too soon after the initial colonization event (Gillespie 2004). For Anolis, this balance is related to island area, the timing of island emergence and species diversification, and island isolation (Losos 2009). For example, the largest island bank, Cuba, is the center of Caribbean Anolis diversity and was likely colonized twice, by the ancestor of most Caribbean Anolis, and possibly to all Anolis (Nicholson et al. 2005), and more recently by a colonist species from Hispaniola, whose ancestor was originally Cuban (Mahler et al. 2010). Cuba thus contains a large amount of phylogenetic diversity, not because it has received outside colonists, but because it is large in area and contains old diverse lineages that have arisen via in situ speciation. Small and spatially isolated banks such as those in the lower Lesser Antilles (e.g., Grenada) have had few ancestral colonizations and few in situ speciation events that together result in low phylogenetic diversity. In contrast, species assemblages on small and non-isolated banks (e.g., the Acklins bank of the Bahamas) are completely derived from among-island colonization’s, and thus, have high phylogenetic diversity similar to the Cuban bank (Fig. 3B). Macroevolutionary simulations should thus be extended to include these isolation effects. However, the model and the Anolis data suggest that, in general, PDARs should be flat for oceanic islands whose species assemblages are an outcome of both in situ speciation and multiple colonizations.”

Figure 4 from Helmus and Ives (2012).

Uta stansburiana mating. Image from http://cabezaprieta.org/

The side-blotched lizard, Uta stansburiana, is one of the most widely-studied lizard species, thanks largely to work by Barry Sinervo and colleagues on the evolution of  alternative mating strategies (a.k.a. the rock-paper-scissors game in lizards).  The most recent report on the evolution of this interesting species investigates reproductive isolation between two populations of Uta that diverged within the last 22,500 years.  One of these populations is found on lava flows and the others if found off the lava flows.  This report by Corl et al. (2012) is noteworthy because recent work on a range of other organisms suggests that some “rules” for the evolution of reproductive isolation are shared across the tree of life.  Do these rules also apply to lizards?

To my knowledge, patterns of reproductive isolation have only been investigated experimentally in one other genus of lizards: Lacerta (Rykena 1991, 1996; Olsson et al.  2004). This work with Lacerta suggest substantial intrinsic reproductive isolation between species resulting from low fertility and high rates of developmental defects in hybrid crosses. Studies of Lacerta also support Haldane’s Rule because females hybrids (ZW) suffer more fitness consequences than male hybrids (ZZ).

By conducting experimental hybridization studies between these two populations of Uta, Corl et al. (2012) were able to show that significant reproductive isolation has evolved between populations, largely in the form of pre-zygotic post-mating isolation; inter-population crosses produce significantly more unfertilized than fertilized eggs relative to intra-population crosses.  Corl et al.’s results are also consistent with at least one general rule for the evolution of reproductive isolation that has been reported in other organisms; asymmetric reproductive of isolation between the two Uta populations is consistent with Darwin’s Corollary to Haldane’s Rule.

How does all this relate to anoles?  My lab is interested in this work because we’re in the midst of a major project designed to answer questions about intrinsic reproductive isolation in Anolis.  Anthony Geneva reported on some preliminary results of this work earlier this year and we hope to have more to report sometime in the near future.

Rykena, S. 1991. Hybridization experiments as tests for species boundaries in the genus Lacerta sensu stricto. Mitteilungen aus dem Zoologischen Museum Berlin 67:55–68.

Rykena, S. 1996. Experimental interspecific hybridization in the genus Lacerta. Israel Journal of Zoology 42:171–184.

Get all the details in the newly posted paper by Eckalbar et al. in BMC Genomics “Genome reannotation of the lizard Anolis carolinensis based on 14 adult and embryonic deep transcriptions,” just posted on BMC Genomics. Here’s the low-down: “The green anole lizard, Anolis carolinensis, is a key species for both laboratory and field-based studies of evolutionary genetics, development, neurobiology, physiology, behavior, and ecology. As the first non-avian reptilian genome sequenced, A. carolinensis is also a prime reptilian model for comparison with other vertebrate genomes. The public databases of Ensembl and NCBI have provided a first generation gene annotation of the anole genome that relies primarily on sequence conservation with related species. A second generation annotation based on tissue-specific transcriptomes would provide a valuable resource for molecular studies. Here we provide an annotation of the A. carolinensis genome based on de novo assembly of deep transcriptomes of 14 adult and embryonic tissues. This revised annotation describes 59,373 transcripts, compared to 16,533 and 18,939 currently for Ensembl and NCBI, and 22,962 predicted protein-coding genes. A key improvement in this revised annotation is coverage of untranslated region (UTR) sequences, with 79% and 59% of transcripts containing 5′ and 3′ UTRs, respectively. Gaps in genome sequence from the current A. carolinensis build (Anocar2.0) are highlighted by our identification of 16,542 unmapped transcripts, representing 6,695 orthologues, with less than 70% genomic coverage. Incorporation of tissue-specific transcriptome sequence into the A. carolinensis genome annotation has markedly improved its utility for comparative and functional studies. Increased UTR coverage allows for more accurate predicted protein sequence and regulatory analysis. This revised annotation also provides an atlas of gene expression specific to adult and embryonic tissues.”