A female A. carolinensis in Ocklawaha, FL moments after laying an egg.
Anyone know of any new phylogeny work on carolinensis? The animals here in Ocklawaha, FL appear so unique. Thin bodied, long limbs. Males are small. I know sagrei pushed them to new heights via rapid evolution, but has this “morph” always been in the forest? Sagrei, I would guess, might be more recent here? Maybe a historic clade that escaped pet trade exploitation? I only see females when they’re down laying eggs. They’re fast and cold give Miami distichus a run for their money.
Ever since the seminal papers by Williams and Rand [1,2], the Anolis radiation across the West Indies has increasingly established itself as an alluring example of ecomorphological convergence. Considering an Anolis community on one island, sympatric species have undergone niche partitioning, whereby each species has evolved particular behavioral, morphological, and ecological traits well-adapted for the microhabitat it occupies. Pop over to another island, and voilà, similar sets of ecomorphs can be found— their resemblance so striking and uncanny.
But the Anolis story isn’t clean cut. Studies of mainland anoles have yielded equivocal findings for whether they also conform to the beautiful patterns observed in the Caribbean. Much baseline data on mainland Anolis communities are needed to determine the extent to which convergence occurs and what factors drive differences in community structure. To partly address this gap, Jonathan Losos, Anthony Herrel, Ambika Kamath, and I recently published a paper describing the ecological morphology of anoles in a lowland tropical rainforest in Costa Rica, at La Selva Biological Station.
Accumulating field observations from four field seasons ranging from 2005 to 2017, we draw from over 1000 observations to characterize the habitat use of eight Anolis species that occur at La Selva. These species include Anolis humilis, Anolis limifrons, Anolis lemurinus, Anolis oxylophus, Anolis capito, Anolis carpenteri, Anolis biporcatus, and Anolis pentaprion, and we opted to devote a brief section to the co-occurring Polychrus gutturosus. Our results revealed overlapping niches and substantial variability in habitat use across many species. Furthermore, the morphologies of A. humilis and A. limifrons were at odds with microhabitat use following the predictions of Caribbean anole ecomorphology. Among the two most abundant species, relative hindlimb length was greater for the more arboreal A. limifrons, whereas it was shorter for the more terrestrial A. humilis.
If mainland and island anoles exhibit divergent ecomorphological patterns, this begs the question of how selective pressures differ between mainland and island habitats to drive these differences. Andrews [3] proposed that predation may more strongly influence Anolis diversification on the mainland, because in comparison to islands, predators are far more abundant, anole population densities are lower, and arthropod prey is plentiful. In contrast, Caribbean anoles are thought to be food limited and there may be stronger selection for niche partitioning. Through examining variation in species’ habitat use relative to the abundance of other co-occurring species at La Selva, our data suggests a low level of interspecific competition for this mainland community, corroborating the hypotheses Andrews set forth.
In recent years, the study of mainland anoles has received more attention. We are in great need of ecological, morphological, and life history trait data for Anolis communities throughout Central and South America to further our understanding of the evolutionary trajectories of mainland and island anoles. So, anole biologists, you can throw out your boats and steer clear of the oceanic divide!
[1] Rand, A. S., and E. E. Williams. 1969. The anoles of La Palma: aspects of their ecological relationships. Breviora 327:1–17.
[2] Williams, E. E. 1972. The origin of faunas. Evolution of lizard congeners in a complex island fauna: a trial analysis. Evolutionary Biology 6: 47–89.
[3] Andrews, R. M. 1979. Evolution of life histories: a comparison of Anolis lizards from matched island and mainland habitats. Breviora 454: 1–51.
Driven by my quest to find Allison’s anoles (A. Allisoni) in the wild, a few weeks ago I dove into a pit of research papers to look for known sightings and/or colonies of A. Allisoni in Florida. I came upon a few vague notations of a colony in Naples with an address included. So, as part of a herping trip for various anoles and lizards to Miami last week, I stopped in Naples along the way.
I drove to the address and, after parking and entering the area, the first thing I saw was a large male specimen of A. Allisoni perched on the side of a palm tree. Shocked and delighted, I snapped a picture.
To see such a beautiful species of anole in Florida in the wild was breathtaking.
The male allisoni was perched on the palm tree with one large male A. sagrei (brown anole) below him. As I approached the palm to get a clearer picture, the sagrei leaped off the palm onto a smaller scrub, and the allisoni followed right after. The two briefly scuffled, nipping at each other before both went their separate ways and I did not see them again.
Strolling around the area to search for more, I found a very small green juvenile anole. It appeared to be allisoni, but did not give me enough time to properly examine it before scuttling up a tree and into the canopy.
Upon returning to the same spot where the first allisoni was, there was another just a few feet away that I had somehow missed the first time. This one had no hints of blue on its head, but simply from its large size, I took a guess that it was an allisoni. After succeeding at capturing it, I took a picture:
Upon first glance, it seemed to be A. carolinensis. However, on a closer look, both the shape of the ear hole and the large scales on the snout suggested allisoni. Here’s a picture of A. carolinensis for comparison:
For the genetics experts reading this, is there evidence of allisoni interbreeding with carolinensis?
Upon revisiting the address the next day, I searched in the same place I found the first allisoni, and, sure enough, found another one, this time suspected to be a female.
Again, I notice the oddly-shaped ear holes and eyes that seem too large for the head, more characteristic of allisoni than carolinensis.
In total, at this colony, I observed four possible A. allisoni, including two adult males, one adult female, and one juvenile.
I plan to return to check for more allisoni before the warm weather ends and anole activity decreases for the winter.
Appearance:Anolis carolinensis is a beautiful green lizard, growing to approximately 8 inches in length, including the tail. Males are larger than females and have proportionally larger heads. The dewlap is usually pink (but can also be grayish or greenish), and is much larger in males than in females. Green anoles can undergo dramatic color changes, from bright green to dull olive, brown, and even yellowish. For this reason, many people in Florida call them “chameleons,” although the green anole’s color-changing ability is modest compared to the true chameleons (Chamaeleonidae) of Africa and Madagascar.
Ecology and Habitat: The green anole’s body shape is that of a trunk-crown ecomorph. But with no other native anoles sharing its range in the southeastern U.S., it historically ranged from the ground to the treetops, making it more of a habitat generalist than Greater Antillean trunk-crown anoles. Today, it shares much of its range with the brown or festive anole (A. sagrei), a Cuban species introduced to Florida around the turn of the 20th century. Many observers believe that the brown anole is driving a decline in green anole populations. This may be true in some places, but another possibility is that green anoles spend more time in the trees where they coexist with brown anoles. In fact, in areas where these two species coexist, the green anole is usually seen on higher perches than the brown anole (which, as a trunk-ground ecomorph, is typically found within a couple of meters of the ground).
Green anoles are active foragers, moving around trees and shrubs in search of prey. They primarily eat insects and spiders, but will also prey on small vertebrates, consume fruit, and even drink nectar from flowers.
Geographic Range and Biogeography: Anolis carolinensis lives throughout the southeastern U.S., from Florida to North Carolina on the Atlantic coast, and west along the Gulf coast through Texas, all the way to the Rio Grande.
Its closest relative is the Cuban trunk-crown species, A. porcatus. Genetic analyses show that the green anole is probably descended from A. porcatus populations from western Cuba, which probably dispersed over water to Florida. The extent of genetic differences between A. porcatus and A. carolinensis suggest that these two species have evolved independently for at least 6 million years, which means that humans played no role in the original colonization of North America by the ancestors of today’s A. carolinensis.
Finally, the green anole itself has become established in many places outside its native range, probably because of its popularity in the pet trade. Today, you can find A. carolinensis in the Pacific (Hawaii, Guam, Palau, and other islands), the Caribbean (Grand Bahama, Anguilla, Grand Cayman), and in southern Japan.
Research Highlights
Anolis carolinensis is a very well-studied species. In a charming 1876 paper titled “The Florida Chameleon,” the Rev. S. Lockwood recounts detailed observations of his pet green anole, a lizard he called “Nolie,” and concludes that the green anole “…is everything that is commendable; clean, inoffensive, pretty, and wonderfully entertaining; provoking harmless mirth, and stirring up in the thinker the profoundest depths of his philosophy.”
Since the late 19th century, biologists have learned a great deal about the green anole, and it has become a model organism for studying many aspects of reptile biology, including the regulation of behavior and reproduction by hormones, social behavior and communication, and the biology of regeneration (because, like most anoles, the green anole can lose and re-grow its tail). In 2011, because of its key role in many subdisciplines of biology, the green anole became the first reptile species to have its entire genome sequenced.
A few recent studies are particularly fascinating. Recall that green anoles coexist with invasive brown anoles (A. sagrei) in parts of their range (see Ecology and Habitat above). In a 2014 study, Yoel Stuart, Todd Campbell, and colleagues studied these two species in Florida by introducing brown anoles to a subset of small, manmade islands that were already inhabited by green anoles. They found that not only did green anoles move to higher perches on the islands they shared with brown anoles, but that over a period of 15 years, the green anoles evolved larger toe pads and more toe pad lamellae (both traits associated with better climbing ability). This may be the best evidence yet that competition between anole species can drive their evolutionary diversification.
Green anoles were in the news again after a 2017 study by Shane Campbell-Staton and colleagues. Studying green anoles in Texas, they measured the lizards’ cold tolerance before and after the winter of 2013-2014, when Texas experienced an abnormally cold “polar vortex” event. Their results show that the extreme cold caused natural selection on the anoles, with southerly populations exhibiting greater cold tolerance after the 2014 polar vortex, on average, than before. Campbell-Staton also used cutting-edge genetic techniques to identify some of the genes that may be involved in cold tolerance.
Appearance: The crested anole, Anolis cristatellus, is a medium sized lizard (50-75mm SVL in adult males) with a stocky body and relatively long limbs. It is light brown in color and both males and females have varying patterns of dark brown on their backs including mottled coloration, hourglass patterns, and longitudinal stripes. As the common name implies, many individuals have a large tail crest (different from the nuchal crest that can be erected in many species), although there is substantial regional variation in this trait and many individuals have no tail fan at all. Dewlap color is typically two-toned with a yellow center and a thick orange outer edge, although some populations have a more monotone yellow-orange dewlap. Females are smaller than males (30-45mm SVL adults) and have relatively small dewlaps. Post-anal scales are not easily visible in this species, sometimes making it difficult to distinguish females from juvenile males.
Within the native range, this species may be confused with Anolis gundlachi and Anolis cooki. Anolis gundlachi can be distinguished from A. cristatellus by the yellow-tipped chin, blue eye, and solid yellow dewlap, but is otherwise similar in size and appearance. Anolis cooki is more difficult to distinguish from A. cristatellus, but the two only co-occur in the dry forests of southern Puerto Rico. In their non-native range in Florida, this species may be confused with Anolis sagrei, which is slightly smaller in size and has a dewlap that is red-orange in the center with a thin band of yellow on the edge.
A. cristatellus male with large tail crest (left) and without (right). Both are in head-down foraging position.
Ecology and Habitat: The crested anole is a trunk-ground ecomorph. It typically perches relatively low to the ground (around 2m high or lower) on broad diameter trees. It is often observed in foraging position on tree trunks with head downward as it sits and waits for insect prey to pass by on the ground. It typically eats insects and spiders, but is also known to consume fruits and to prey on small vertebrates, including anoles of their own and other species. This species is rarely seen on the ground except for when moving between perches or catching prey. Like other trunk-ground ecomorphs, A. cristatellus, has relatively long limbs and a stocky build ideal for quickly navigating both arboreal and ground habitat. Anolis cristatellus is commonly found at lower elevations in warm forest habitats and is often restricted to edge or open, disturbed forest habitat at cooler, high elevations. This species is the most common and abundant anole in urban areas in Puerto Rico.
Body size differences are the easiest way to differentiate adult female (left) and male (right) A. cristatellus. (Photo by Kristin Winchell)
Geographic Range and Biogeography: Anolis cristatellus is endemic to the Puerto Rican bank (Puerto Rico and the Virgin Islands). Its closest relative is A. desechensis, which is found only on the island of Desecheo off the west coast of Puerto Rico. It is also closely related to A. scriptus (found in the Turks and Caicos), A. cooki (found in dry forests in the southwest of Puerto Rico), and A. monensis (found on the island of Mona off the coast of Puerto Rico). Genetic analyses indicate that the ancestor to A. cristatellus (and 12 other Puerto Rican species, which make up the “cristatellus” group) likely colonized Puerto Rico from Hispaniola at least 40 MYA. More recently, A. cristatellus has established in several places outside of its native range, facilitated largely by sale of tropical plants. In particular, it is established in Miami (Florida), Dominica, Costa Rica, Mexico (Yucatan), Trinidad, Saint Martin, and the Dominican Republic.
Research Highlights:
Anolis cristatellus is a great study species for answering so many different questions! As the most wide-ranging Puerto Rican species, it is perfect for comparative studies. Researchers have found no end to the questions they can answer by examining variation within A. cristatellus in different environments and between A. cristatellus and other Puerto Rican species.
An urban A. cristatellus male perched on a metal fence in Puerto Rico. (Photo by Kristin Winchell)
Appearance: Anolis distichus, the bark anole, is a medium sized anole with a body color that varies from gray, to brown, to green – depending on the population. Body coloration is similar in both sexes but females can be distinguished from males by their lack of a dewlap, smaller adult size, and a relatively flatter head than males. Male dewlap color in this species is widely variable with populations ranging from pale white or yellow, to populations with variably sized red or orange spot in the center, to populations with entirely red or orange dewlaps. Bark anoles co-occur with a variety of species, most of which can be easily distinguished as different ecomorphs with larger heads or bodies such as Crown Giant and Trunk Ground anoles, or more slender frames such as of Trunk Crown, Grass Bush and Twig anoles. In Haiti and the Dominican Republic, the range of bark anoles overlaps with those of other closely-related trunk anole species – Anolis brevirostris, Anolis caudalis, Anolis marron, and Anolis websteri. These species all have a black spot on their neck, which is lacking in Anolis distichus.
Ecology and Habitat:Anolis distichus are trunk anoles, an ecomorph with a compact body plan – short snout and tail, with a relatively wide midsection. Trunk anoles like Anolis distichus primarily occupy the vertical surfaces of trees, usually below the canopy. They are found in a wide variety of natural habitats including xeric scrub to mesic humid forests as well as human-created habitats like buildings, parks, fruit tree groves, and residential areas. Unlike other ecomorphs that flee up trees or run to the ground when approached, bark anoles often shimmy to the opposite side of the trunk, a behavior commonly referred to as “squirrelling”. Bark anoles will eat nearly any prey that can fit in their mouth but their primary diet includes small arthropods like crickets, beetles, and even bees! Bark anoles are especially fond of ants.
Geographic Range and Biogeography: Bark anoles are native to Hispaniola (Haiti and the Dominican Republic) and the central Bahamas. Although they were once considered native to Florida, genetic data suggests these populations are the result of multiple introductions from Hispaniola and the Bahamas some of which occurred at least 50 years ago. They are thought to be introduced to Abaco Island in the northern Bahamas, but fossil evidence of this species on Abaco puts the status of this population into question. Phylogenetic evidence finds that bark anoles arose on the northern paleo-island of Hispaniola, dispersed over-water to colonize the the Bahamas, and spread to areas of to the southern Hispaniolan paleo-island after the two paleo-islands fused to form present day Hispaniola.
The immense variation in body and dewlap color in bark anoles has led to the description of 18 subspecies of Anolis distichus. Research currently underway seeks to understand if these subspecies are in the process of speciation or have perhaps already achieved species status.
Research Highlights:
Bark anoles have long been the intensive research effort with particular interest in using bark anoles to understand 1) the evolution of signals and 2) the process of speciation.
Most anole species possess and make extensive use of their colorful dewlaps for signaling to each other as well as other species. A series of studies led by Julienne Ng has shown that dewlap color is a heritable genetic trait and is associated with signaling environment that animal occupies. Exciting research, currently underway by Winter Beckles, seeks to understand if bark anole populations shift their dewlap color in response to changes in their light environment caused by hurricanes.
Julienne Ng has also found that some subspecies with different dewlaps interbreed freely over a wide geographic area. In contrast, other subspecies pairs are confined to a narrow hybrid zone suggesting that, for these subspecies pairs, hybridization may have negative fitness consequences and those populations may be in the process of speciation. Research I performed as part of my dissertation also found that transitions in dewlap color are associated with diversification events suggesting dewlap divergence may play in role in driving or maintaining speciation events. We also found evidence found that there are more distinct lineages that previously recognized within the Anolis distichus group and one subspecies in particular – Anolis distichus dominicensis is actually three separate lineages. Work I performed with undergraduate researcher (now Yale PhD student) Daniel MacGuigan used multispecies coalescent methods to assess if Anolis distichus represents a single species or multiple species. We found support for at least seven distinct species in the group, but at present we have not updated the taxonomy because the boundaries between these species remain unclear, particularly for the separate lineages of A. distichus dominicensis.
Appearance:Anolis sagrei may not be the most colorful or strikingly patterned anole, but owing to its widespread distribution and high abundance it may the anole most familiar to you. Adults commonly grow to 7-8 inches from head to tail with females being a few inches smaller than males. Their body color ranges from light tan to gray to dark brown, almost black. Unlike green anoles that can turn brown, these guys are never green! Males have red-orange dewlaps, sometimes with a yellow border or blotches. Females often have a pattern with diamonds, bars, or a stripe running down their back. When in south Florida don’t confuse brown anoles with crested anoles (Anolis cristatellus). Crested anole females only have a cream-colored stripe on their backs, and brown anoles do not have a light ring around the eye or a light stripe above their front limb. Brown anoles often have two dark bars above their eyes.
Ecology and Habitat: The brown anole is a trunk-ground habitat specialist or ecomorph. They are often found on the ground or perching low on tree trunks (up to 1.5 m high). Brown anoles have relatively long limbs for their body size, which allows them to run fast on the ground and tree trunks that they typically occupy. Brown anoles are usually sit-and-wait foragers, keying in on the movement of prey to jump from their perch and attack. Their diet consists of a wide variety of arthropods including most any spiders and insects they can fit in mouths. They will occasionally eat other invertebrates and small vertebrates including their own hatchlings. Brown anoles primarily occupy disturbed and edge habitats in both natural and human-modified landscapes. Their abundances suggest they are just as at home in the city as in natural areas. Like tourists at the beach, these guys love the sun – they are often active during the hottest parts of the day. All anole species display, but brown anoles are the champions – they are often seen fanning their brightly colored dewlaps, and doing head-bobs and push-ups with the intensity and stamina of an Olympic athlete.
Geographic Range and Biogeography: The native range of the brown anole includes the Bahamas, Belize, Cuba, Cayman Brac, Little Cayman, Swan Island and the Gulf of Mexico/Caribbean coast of Mexico. Its evolutionary origin as part of the 15-species sagrei group is Cuba with multiple colonization events to Caribbean islands east and west of Cuba to round out its native range. One of the best natural colonizers of all anoles, brown anoles are also the undisputed champion of recent human-mediated introductions. Non-native populations are well established around the world including the southeastern United States (e.g. Alabama, Florida, Georgia, Texas), Atlantic islands (e.g. Ascension, Bermuda), Caribbean islands (e.g. Grand Cayman, Grenada, Jamaica, St. Vincent), and Pacific islands (e.g. Hawaii, Taiwan), among other locations with reports of new introductions every year. Genetic analyses reveal multiple origins of these introduced populations from numerous localities in Cuba as well as the Bahamas and Belize. A key discovery about these introductions is that genetic variation from these multiple native-range sources mixes within non-native populations, resulting in increased genetic variation compared to native-range populations.
Research Highlights:
If Anolis carolinensis (green anole) is the “lab rat” of the reptile world, then Anolis sagrei is undoubtedly the “field rat.” This species has been studied extensively in the field from populations on small islands in the Bahamas to the heart of the city in Miami. A well-studied natural history, high local abundance, and the ability to tag individuals for unique identification make this species ideal for field studies of natural selection. We have learned that natural selection acts on morphological, physiological and behavioral traits of brown anoles. For example, natural selection favors longer hindlimbs in the presence of terrestrial predators (curly-tailed lizards, Leiocephalus carinatus) and higher optimal performance temperatures in warmer habitats. Other studies show adaptive responses of limbs to local vegetation after being introduced to new islands. A recent study by Oriol Lapiedra and colleagues evaluated whether natural selection acts on variation in risk-taking behavior of brown anoles when they occupy small islands with and without the ground predator Leiocephalus carinatus. Brown anoles that avoided the ground in lab trials were favored in the presence of the predator, whereas more exploratory brown anoles survived better in the absence of the predator. Moreover, selection on behavior and morphology acted independently. This experiment is among the best studies yet showing that natural selection acts on behavior.
Brown anoles are also a key species in studies of the consequences of global environmental change, including biological invasions, climate change, and urbanization. Recent studies of non-native brown anoles in Miami by Jason Kolbe and his lab discovered that brown anoles living in the city have consistently different personalities compared to their forest counterparts – city lizards are more tolerant of humans, less aggressive, more exploratory in new environments, and bolder after simulated predator attacks. Cities also dramatically alter the ecological niche space occupied by brown anoles. Urban heat islands produce warmer microclimates that allow brown anoles to more often attain their preferred body temperatures during the summer in Miami, likely increasing their ability to persist in some areas. Brown anoles prefer to perch on broad substrates like tree trunks, and urbanization typically results in the removal of smaller trees and the addition of broad diameter artificial structures, such as light posts and utility poles. This leads brown anoles to use broader perches in urban areas despite the fact these artificial substrates are often quite smooth and lizards slip and fall when using them.
