Allopatric Speciation in the Caribbean Anolis – Literature Review “The Origin of Species: Lizards in an Evolutionary Tree”

Ingrid Schoonover

October 31, 2020

The literature in reference is titled “The Origin of Species: Lizards in an Evolutionary Tree” and can be viewed at this link: https://www.biointeractive.org/classroom-resources/origin-species-lizards-evolutionary-tree

Jonathan Losos and Sean B. Carroll were studying Anoles in the Caribbean to understand how adaptations arise and how new species form. The researchers in the videos used the biological species concept to define species as groups that are reproductively isolated from other species.  On the Caribbean islands, the anoles species share a general space and diet but divide up the habitat by height, so that each species lives at a different elevation. At ground-level and at the bottom parts of tree trunks the trunk-ground anole can be found, it is longer-legged than the other anole species and is a bit stockier. The grass-bush anole is found higher up on the grasses and bushes, it is a slender species with a long tail. Further up in the trees on small branches and twigs the twig anole can be found, it is a very slender anole with short legs. The canopy anole occupies the tallest point of the canopy, it is a large green lizard with toe pads that are quite large in proportion to its body size. The phenotypic variation in terms of leg length and toe pad size by species in each microhabitat suggests that these are adaptations to the environment, but it needs to be tested to see if they are actually adaptations through an experimental, observational, or comparative method. An adaptation is a character change that increases the animal’s probability of survival, it is the product of natural selection acting on a genotype in a way that results in a higher probability of survival and reproductive success for a population in each environment. Sean and Jonathan designed two simple experiments to test if leg length and toe pad size are in fact adaptations.

In the first experiment the running and grasping ability of long legged and short legged lizards was compared on broad and narrow branches. On the broader surfaces the trunk-ground anole sprinted quickly up the branch, while the twig anole was very slow and barely inched up the large branch. So, in terms of speed on broad surfaces, the long legs of the trunk-ground anole are an advantageous characteristic and short legs of the twig anole are a disadvantage. When the anoles were placed on a much thinner branch then the twig anole was able to firmly grasp the branch and balanced well, on the other hand, the trunk-ground anole was very clumsy and looked like it was going to fall off. In this environment, the short legs of the twig anole are advantageous because they provide good balance, but the long legs of the trunk-ground anole are disadvantageous because they increase the risk of falling and are poor for balancing. In conclusion, longer legs are an adaptation for environments that require speed and have broader surfaces such as near the ground, and shorter legs are an adaptation for environments where balance is more important than speed such as higher up on a tree. This means that leg length in anoles is an adaptation to different environments. This makes sense because the trunk-ground anole lives at the bottom of trees and needs to run to the ground quickly to catch prey, whereas the twig anole lives on thin branches and twigs so it is paramount that it can balance well to ensure it does not fall out of the trees.

The second experiment explored the relationship between toe pad size and leaf climbing ability to determine if toe pad size was another adaptation. They placed the trunk-ground anole with small toe pads and the large canopy anole with large toe pads on a smooth leaf and watched them to see how well they could climb up it. The trunk-ground anole had a very difficult time hanging onto the smooth surface of the leaf and fell off of it, however, the canopy anole climbed the leaf very well because the microscopic hairs of the toe pad bonded to the surface allowing it to scale the leaf even though it is bigger and heavier than the ground anole. This confirmed that enlarged toe pads are an adaptation for hanging onto surfaces, which is critical to species that live in canopies because if they slip and fall, then they would die.

Sean and Jonathan wanted more evidence that leg length was actually an adaptation and not just a made-up story, so they decided to use the rapidly changing environment of small Caribbean islands as labs to observe the evolution of adaptations because these islands are devoid of lizards due to frequently occurring hurricanes. They captured long-legged tree-dwelling anoles from the larger island and then introduced a male and female anole to 7 islands that hurricanes have cleared of lizards, these islands have no trees and instead just have small bushes with thin branches. A year later the researchers returned and discovered that the original pairs of anoles survived and reproduced on the islands, with the new populations living on thinner branches. They took baseline data that measured how far the anoles were off the ground, the diameter of the surface they were perched on, and the position that they were perched. They brought the anoles back to the lab and took x-rays that mapped their leg length and they scanned the toe pads. When they returned a year later, they discovered that in just two generations the average leg length had shortened. Over the next four years, their legs became shorter and shorter. This is an example of dispersal under the allopatric model of speciation, where a subpopulation of the long-legged anoles is removed from the main populations and then isolated on smaller hurricane-prone islands via forced migration by the researchers. In their previous environment their longer legs were an advantage for climbing quickly on broad branches and the trunks of trees, but this presents a disadvantage on these smaller islands devoid of trees. Natural selection acts strongly on genetic drift in the small island populations within this new environment to rapidly select for reduced leg length in the anoles over generations, this is an adaptation that allows them to better grasp the thin branches of the short bushes found on the small island.

These adaptations only explain how different phenotypes arise, but not how a new species of anole arises. Two groups or populations of anoles can be defined as unique species when they are reproductively isolated, either from prezygotic isolation that prevents mating from occurring in the first place or postzygotic isolation where gene flow is prevented after a hybrid species is formed by reinforcement through hybrid inviability, sterility, or decreased fitness in the hybrid offspring. Some mechanisms of prezygotic isolation include ecological isolation, temporal isolation, microhabitat isolation, behavioral isolation, or morphological isolation. For speciation to occur a population needs to get isolated in the first place, such as by vicariance when an original population is divided geologically into two subpopulations or by dispersal as discussed before with the anoles on smaller islands. The allele frequencies in the subpopulations will be different from the original population by chance alone due to random sampling error, this is known as genetic drift. Natural selection acts on this genetic drift and the new environmental pressures that come with the new habitat which quickly results in divergence, where the two populations become more and more different over time. This process can also be sped up by assortative mating, or differences in mating preferences by population due to sexual selection. Then the final step to speciation is if or when the species come into secondary contact they do not reproduce and form viable offspring.

For anole populations in secondary contact with each other it is often behavioral prezygotic isolation where sexual selection maintains reproductive isolation. Anoles are sexually dimorphic, each species of anole in the same area has a differently colored dewlap, which is a flap of skin under the throat that males display to attract female mates of the same species. The unique colored dewlap of each species means that females will only recognize a specific color as a male of their own species and will not mate with other species or populations displaying a different color dewlap. Male anoles displaying their brightly colored dewlap to females is an example of female choice sexual selection on males, where the females drive the evolution of a certain phenotype in males (in this case dewlap color) based on preference.

For example, the bush-grass anole has a lightly colored dewlap that contrasts well with the dark forest, the females find this contrast impressive, so they chose to mate with the males that have the dewlaps that contrast with the environment. However, if a subpopulation of the bush-grass anoles were removed and placed in a sunny open habitat then the lightly colored dewlap would not be as effective at impressing females, and in this habitat males with a darkly colored dewlap would attract more female mates. Overtime, the higher fitness of the darkly colored dewlap males in the sunny environment would drive the evolution of dark dewlaps in the population. It is possible that the ideal dewlap could be an indicator of better genes where the males with the ideal dewlap produce offspring with higher fitness. More likely, this appears to be an example where females find some arbitrary trait more exciting perhaps because it has an intrinsically stimulating response on the nervous system, this sexual selection acts on a pre-existing sensory bias for contrasting colors. This can lead to runaway selection, where the offspring also inherit the genes for this arbitrary female preference and chose to mate with anoles that have the same phenotype as their father, which in turn increases the display of this phenotype in the males and extenuates the condition over time. Females push the males into extremes which rapidly leads to divergence due to genetic drift of the subpopulation, and reproductive isolation soon follows because males without this dewlap characteristic are less reproductively successful. Then, by some chance if the lightly colored dewlap anoles and the darkly colored dewlap anoles were brought back together in the same area, the females of one population would fail to recognize the males of another population due to the differently colored dewlap so they would not mate, thus the two populations become two species due to reproductive isolation. Thus, the formation of a newly colored dewlap or the origin of other forms of reproductive isolation can rapidly lead to the formation of new species, and then between species competition for resources can drive the evolution of different body types. Natural selection acts on populations or species in such a way that favors the occupation of various niches where there are more resources available. When a species becomes more adapted to one niche over another, then a different type of prezygotic isolation maintains reproductive isolation, and this is called microhabitat isolation. Microhabitats can reproductively isolate species because they never encounter one another and thus do not have the opportunity to mate.

While studying the anoles on Puerto Rico, Jamaica, Cuba, and Hispaniola the researchers realized they were finding the four same basic body plans: trunk-ground anoles with long legs, bush-grass anoles that are slender with long tails, twig anoles with small bodies and short legs, and canopy anoles with large toe pads. They were then faced with determining whether the identical character states among each type of anole on the four islands were caused by homology or homoplasy. Homology is the result of multiple groups inheriting a characteristic from a shared common ancestor with the same characteristic, meaning that they would all be in a plesiomorphic state. If this was the case, then grass-bush anoles on one island should be more closely related to the grass-bush anoles on another island than they are to canopy anoles of the same island and so on. On the other hand, homoplasy is the result of the same character state arising independently in multiple groups or lineages, and where the character state is not found in the shared common ancestor, meaning the groups are in an amorphic state. If this was the case, the anoles of one body type should be more closely related to anoles of a different body type on the same island than they are to anoles of the same body type on another island.

To determine which explanation was the most likely they sequenced the DNA of anoles from each island and examined the same stretch of DNA for each body plan to determine the evolutionary relationship between them. They placed the body type of anoles from each island at the terminal nodes and then joined them with internal nodes showing degrees of common ancestry based on which two terminal nodes were the most closely related, meaning which two taxa had the least number of base pair substitutions between them. They continued this process of joining nodes internally until a complete phylogenetic tree was constructed, which showed the evolutionary relationship of the anoles because more divergence between taxa should correspond to evolutionary time. This phylogenetic tree revealed that the anoles on the same island were more closely related to each other than they were to similar looking anoles of other islands, this means that each of the four body plans evolved independently on each island. This means that the four anole types within each island descended from a shared common ancestor and thus form monophyletic groups. On the other hand, combining all the similar looking anoles from the four separate islands would form a paraphyletic group because some of the descendants from the shared common ancestor were excluded. Furthermore, this methodology of constructing a phylogenetic tree to study the adaptive significance of traits is also an example of the comparative method of testing adaptations. This method increases the confidence of the hypothesis that leg length and toe pad size are in fact adaptations because the most recent common ancestor for the anoles is island-specific which means the traits are independent and arising through homoplasy. Specifically, this would be an example of parallelism, a type of homoplasy where the same character state is derived in several lineages independently from similar common ancestors that did not share the same character state.

Citations

Losos, Jonathan. Lizards in an Evolutionary Tree. Berkeley, CA: University of California Press, 2011.