Males and females of many species vary in their morphology, behavior, and physiology. Whether exaggerated weapons, elaborate coloration patterns, or dramatic differences in size, these sexual dimorphisms form some of the most eye-catching elements of biological diversity. These striking differences are often considered as a product of sexual selection, whether due to direct female choice for an elaborate structure or traits used by combative males to assert dominance. But additional patterns of dimorphism become visible with quantitative comparisons of male and female body proportions, which may yield additional clues to ecological differences between the sexes. Considering that patterns of sexual dimorphism can diverge rapidly among species it is no surprise that they have intrigued biologists since before Darwin.
Anolis brunneus from Crooked Island, Bahamas. A member of the carolinensis clade of anoles exhibiting extreme levels of facial length dimorphism.The male is the large lizard to the bottom left, the female to the upper right.
Anolis lizards offer a mosaic of conspicuous and subtle dimorphisms that vary extensively among species. Some dimorphisms, such as dramatic differences in body size, differences in dewlap color, or differences in display behavior, are readily visible in anoles. But anoles also exhibit subtle differences in body proportion that may have important ecological correlations. These dimorphisms have been the subject of several studies by Marguerite Butler, Jonathan Losos, and Michele Johnson. But as I have commented here in the past, variation in head dimensions have rarely entered into the oft-told stories of anole ecology and evolution, including discussions of sexually related variation. In a forth-coming study to be published in the journal Evolution I, with the assistance of Emma Sherratt, Joel McGlothlin, Butch Brodie III, Arhat Abzhanov, and Jonathan Losos, explore the patterns of craniofacial dimorphism of Anolis lizards over both evolutionary and developmental time scales.
Male and female skull diversity of Anolis lizards. Note that many species vary greatly in size, but to a lesser degree in skull shape. All except for the carolinensis and hendersoni anoles that is.
For this project we began by quantifying sexual dimorphism in head shape for 50 species of Anolis lizard. This analysis uncovered that most species have relatively low levels of head shape dimorphism. But two groups of species, the carolinensis and hendersoni clades, have independently converged on extreme levels of dimorphism through nearly identical changes in male facial morphology. In each of these distantly related clades males have evolved extraordinarily long faces while females retain faces of more moderate proportions. Compared to evolutionary patterns of convergence in other traits that are associated with anole ecomorphology, this pattern comes as a surprise because the carolinensis and hendersoni clades occupy very different microhabitats. The carolinensis anoles often occupy green, leafy vegetation relatively high in canopy of Cuba and the surrounding islands. In contrast, the hendersoni anoles occupy fern covered mountainsides in Haiti and the western Dominican Republic. The selective bases of this convergence on similar patterns of sexual dimorphism – not just morphology, but sex-specific changes in head shape – remains a mystery.
Among vertebrates differences between males and females can arise prior to hatching/birth, such as for the primary reproductive organs or the 2:4 digit ratio, or later in life, such as for the emergence of human body hair or breast enlargement. Therefore, to understand whether convergent patterns of sexual dimorphism evolved through similar developmental strategies it is first critical to understand the timing of sexual differentiation. Comparison of the carolinensis and hendersoni clades revealed that they develop their sexual dimorphism through distinct developmental strategies; dimorphism in the carolinensis anoles emerges around the time of sexual maturity and continues to increase late into life while dimorphism in the hendersoni clade develops early and is maintained at a constant level through later stages. Comparing these developmental patterns across an array of species with varying levels of facial dimorphism later revealed that the extreme dimorphism of the carolinensis clade is actually the result of an evolutionarily novel developmental change that occurred somewhere near the base of this clade. As suggested by the morphological comparisons, this developmental shift also appears to be male specific. Extreme dimorphism in the hendersoni clade results from the exaggeration of a broadly shared, likely ancestral, developmental strategy.
Alternative developmental models of sexual dimorphism. Like most anole species, the hendersoni anoles exhibit the early divergence. In contrast, the carolinensis anoles exhibit late divergence, not significantly diverging in head shape until around sexual maturity.
As biologists seeking to explain biological diversity through various mechanistic scenarios, our study illustrates well how layering developmental analyses upon morphological and ecological comparisons can open new lines of inquiry. The extreme dimorphism in the hendersoni clade sits at the end of a developmental continuum with other anole species. This may suggest that the same selective scenario is at play among most anole species, that varying levels of dimorphism simply reflect varying intensities of selection on a common developmental background. The hendersoni anoles also illustrate that internal constraints associated with facial development do not impede the evolution of extreme dimorphism within the ancestral developmental strategy. Something may be peculiar about the carolinensis anoles, however, as their unique developmental strategy may suggest that a previously unfelt selection pressure has restructured the developmental-genetic architecture of this clade. The continual divergence of the sexes throughout their reproductive stages may also suggest something about the nature of the selection pressure, perhaps suggesting a role for sexual selection over natural selection. Unfortunately, at this time there is little data available to test between alternative hypotheses regarding the origins of anole head shape diversity and sexual dimorphism. Regardless, once again Anolis lizards force us to accept that that the factors underlying the generation of biological diversity may be more complex than we might have initially thought.
Sanger TJ, Sherratt E, McGlothlin JW, Brodie ED III, Losos JB, Abzhanov A.
Convergent Evolution of Sexual Dimorphism in Skull Shape Using Distinct Developmental Strategies. Evolution in press.
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- The Super Sticky Super Power of Lizards: a New Outreach Activity for Grade-Schoolers - April 9, 2018
- Updates on the Development of Anolis as a “Model Clade” of Integrative Analyses of Anatomical Evolution - September 4, 2017
Skip (James) Lazell
What about Anolis pulchellus? Males just bigger? Skip
Thomas Sanger
Hi Skip, A. pulchellus wasn’t in our morphometric analysis because the MCZ does not have any females skeletonized. However, in the previous study I published on male skull shape variation A. krugi and A. pulchellus had very similar head shapes so it would be surprising to me if they varied highly in sexual dimorphism.
All that being said, A. pulchellus was included in our allometric study of facial length dimorphism. Without dredging up my data and just eyeballing Figure 4 it appears that A. pulchellus has about half of the dimorphism as A. hendersoni. My hunch is that the large size dimorphism of A. pulchellus creates the false appearance of also having a lot of shape dimorphism. This was also a common misconception among primatologists until Cheverud and colleagues quantified the variation.
Skip (James) Lazell
Thanks!