Divergence and Speciation in the Lesser Antilles

Fig. 1 from Muñoz et al.: Anolis marmoratus subspecies on Basse Terre (left) and Grande Terre (right)

Fig. 1 from Muñoz et al. (2013) Anolis marmoratus subspecies on Basse Terre (left) and Grande Terre (right)

Unlike the extensive within-island speciation that anoles have undergone in the Greater Antilles, we have no evidence that the same has occurred in the Lesser Antilles. Rather, Lesser Antillean islands that contain two species are thought to be the result of dispersal events rather than in situ cladogenesis. Despite such low species diversity, however, phenotypic diversity on many of these islands certainly is not lacking. Some Lesser Antillean anoles exhibit spectacular geographic variation in head, body and dewlap colouration and pattern, as well as body size and scalation, that appears to be adaptive to different environments. So, while this variation has not led to complete speciation in any Lesser Antillean anole, is there some evidence that these phenotypically divergent populations are at some stage of the speciation process? Also, how does phenotypic divergence occur on these smaller islands when there seems to be little opportunity for geographical isolation?

AA contributor, Martha Muñoz and colleagues tackle these very questions in a recent paper in Molecular Ecology. Muñoz et al. focus on the stunning phenotypic diversity of the Anolis marmoratus complex on Guadeloupe, which has been categorised into 12 subspecies. On Grande Terre, in particular, two subspecies can be found: A. m. speciosus inhabits mesic habitats in the southwest and A. m. inornatus inhabits the xeric lowlands of the north and east. Males share a yellow-orange coloured dewlap but differ in head, body and eye ring colouration, while females and juveniles of the two subspecies are similarly drab in colour.

To investigate colour divergence and speciation in these two phenotypically divergent subspecies, Muñoz et al. use microsatellite markers and phenotypic and habitat reflectance data sampled across two transects. Their results show that first, change in colouration coincides with the mesic-xeric ecotone on Grande Terre. Curiously, the divergent colouration may actually be due to two different selective forces. The green body, and blue head and eye ring of A. m. speciosus stands out from the background suggesting that colouration in this subspecies may be driven by sexual selection. On the other hand, the duller colouration of A. m. inornatus is similar to the background suggesting that selection is driving crypsis in this subspecies.

Second, Muñoz et al. find that there has been a history of continual migration between the two subspecies and large effective populations sizes. This suggests that divergence in colouration has occurred in the face of gene flow (i.e. parapatric divergence), rather than the alternative model of divergence in geographic isolation followed by secondary contact.

Lastly, the pattern of gene flow throughout their history does not appear to have stopped. Muñoz et al. find that contemporary rates of gene flow are high despite clear differentiation in colour, suggesting that strong divergent natural selection is maintaining colour differentiation between the two subspecies while gene flow is homogenizing neutral regions of the genome (presumably where the microsatellite loci are).

This study is aligned with studies by Thorpe’s group on A. oculatus on Dominica and A. roquet on Martinique, which show that speciation has not reached the point of completion in Lesser Antillean anoles despite extensive adaptive variation in phenotype. However, Muñoz et al.’s results shine light on the possibility of parapatric divergence in anoles. So, if parapatric divergence is possible, what then is inhibiting speciation in the Lesser Antilles? Why does there appear to be a threshold island size of 3000km2 for within-island anole speciation to occur, as Losos & Schluter’s (2000) study proposed? A comparative approach and more fine-scaled studies on both the Lesser and Greater Antilles will certainly help move us towards elucidating the conditions required for anole speciation to reach the point of completion.

About Julienne Ng

I study the evolution of color signals. My PhD at the University of Rochester focused on the evolution of dewlap diversity in Anolis distichus. I am currently a postdoc at the University of Colorado studying the evolution of flower color.

9 thoughts on “Divergence and Speciation in the Lesser Antilles

    1. Hi Skip,
      Your 1963 and 1972 bulletins have followed me around for the last 7 years! You definitely presaged many of our findings.
      Best,
      Martha

  1. The inferences about the different selective forces influencing the coloration in the two subspecies reveal the foresight of the authors who named them (Garman and Lazell, the author of the previous comment): speciosus = L. beautiful, splendid, showy; inornatus = L. unadorned.

  2. This case seems like an opportunity to redefine or defend the use of subspecies as distinctive morphs that are maintained by natural selection in the face of gene flow. —
    ———-
    And hurray for André Schneider (Chris’s son) for being a high school student co-author.

    1. Hi Todd,
      Interesting point and I totally agree. Also, not only did Andre help us by collecting lizards and editing the MS, but he also is a burgeoning photographer. Several of the shots in Figure 1 (above) were his!
      Best,
      Martha

  3. Julienne –
    Thanks so much for the lovely recap of our paper. Your 2011 study with Rich featured prominently in the interpretation of our results and the readers of this blog who are interested in this type of work should definitely have a look!
    Best,
    Martha

  4. Martha,

    Really cool stuff! As I was reading, I was curious about whether there might be a significant environmental component to color variation in this species. It seems like it would be a long shot (given what is known generally about the genetics of coloration and the large differences between these subspecies), but could a G X E interaction be part of what drives these differences you saw? As you say in the paper, they are in dramatically different environments.

    -Mike Logan

  5. Hi Mike,
    Great question! The genetic basis of coloration is a huge line of research. Nick Crawford will be giving a talk at Evolution on his work searching for the genes underlying dewlap coloration, actually. From what is known about coloration in anoles, it seems that differences we observed are likely not highly influenced by environment. The blue of A. marmoratus specious derives from a structural pigment, and so we wouldn’t necessarily expect it to be environmentally influenced. We also found quite a bit of variation in yellow, which could represent differences in sequestered carotenoids. However, a study by Steffen et al. (2010) found that varying carotenoid content did not alter the color of A. sagrei’s dewlap. This species dewlap contains red and yellow, and so it could have been sensitive to sequestered pigments (i.e., carotenoids). All in all, much of the coloration differences observed are likely due to genetic differences. There could be some environmental component, and until we have more data we can’t be completely sure, but all the available evidence suggests that genetic differences among populations forge the color cline. We address this point briefly in the Discussion, but the topic merits more attention.

    Best,
    Martha

    Steffen JE, Hill GE, Guyer C (2010) Carotenoid access, nutritional stress, and the dewlap color of brown anoles. Copeia, 2010, 239–246.

    1. Right, that makes a lot of sense. It definitely seems intuitive that the kinds of color differences you’re seeing would have a large genetic component, but I was just curious. Thanks Martha!

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