We’ve had previous posts on parasites of anoles (for example, here), but now a new paper in Herpetology Notes adds to the literature on this topic, reporting blowfly parasitism of Anolis parvauritus from northwest Ecuador.
Transposable elements are DNA sequences that move around in the genome. Do they also play any roles in evolution and development? I answered this question by looking at our favourite group of animals – lizards – and found some surprising answers. My most recent paper in Evolution Letters is the last of a trilogy of papers – one, two, and three – that reveal that Anolis lizards, by breaking the rules, allow us to link TEs to speciation and evolvability.
Mobile DNA sequences – transposable elements or TEs for short – are found in the genome of virtually all organisms. As their name implies, TEs can cut or copy themselves from one location in the genome to another. This can wreak havoc as insertion of TEs may interfere with gene regulation or in fact knock out entire genes. Cells therefore have mechanisms that prevent TEs from jumping, including DNA methylation and other epigenetic tools. Thus, TEs are not roaming freely through the genome, but are restricted from entering functionally important parts. Preventing TE invasion is particularly important when genes are regulated through spatial proximity to each other. The textbook example of this situation are the Hox genes, which are the key players in embryonic development with an ingenious mode of action: Hox genes are arranged in tight clusters and their position in the cluster defines their time and space of expression, and thus their effect on the patterning of the early embryo. It is therefore fitting that Hox gene clusters of mammals and other well-studied vertebrates have been found to be almost completely free of TEs. My new study reveals that Anolis lizards have broken this paradigm. Moreover, the invasion of TEs into Hox clusters of Anolis lizards can be linked to aberrant gene expression and increased rates of speciation.
Ever since the discovery of TEs, people have speculated about their evolutionary implications. One possible consequence of high TE activity is structural genomic variation. This may accelerate genomic incompatibility between populations, effectively making TEs engines of speciation.
Occasionally, TE insertions may also generate phenotypic novelty. As noted above, some genes are regulated through their proximity to other genes, which means that invasion of TEs can change expression of a number of genes simultaneously. Furthermore, since jumping TEs often drag along neighbouring genomic regions, they can translocate regulatory sequences that cause genes to be expressed in new cell types or at different stages in development.
While these are good reasons to expect TEs to promote evolution, examples are few and their role often appears idiosyncratic. An excellent group for a more systematic survey of TE-driven diversification is squamate reptiles, a group that includes lizards and snakes. Squamate genomes do not only appear particularly rich and variable in TEs, but their body plan is also highly malleable. Illustrative examples include the adaptive radiation of Anolis lizards and the repeated evolution of limbless and elongated bodies.
I decided to study how TEs have shaped the genomes, and in particular, the Hox clusters, of squamates. My first surprise was to discover that lizards possess more Hox genes than all other tetrapods since they retained some genes that other lineages have ditched. The second surprise came when I looked at the TE content of Hox clusters. Despite the high TE content in their genomes, squamates follow other vertebrates in generally protecting their Hox clusters from TEs. But there was one exception: I found massive invasion of TEs in the Hox clusters of two out of three Anolis species, with TE contents almost as high as the average place in the genome.
The relationship between TE content in Hox clusters relative to genome-wide TE content in squamate reptiles. All lizards and snakes restrict TEs from their Hox clusters down to roughly half the genome-wide average. However, two Anolis species show Hox clusters that are invaded by TEs, while a third Anolis species (black circle) follows the general trend.
Why in Anolis? Anolis lizards are famous in evolutionary biology due to their adaptive morphological radiation involving high rates of speciation – amassing close to 400 species. In a previous study (explained in a previous Anole Annals post) I showed that Anolis lineages with more speciation events in the past have more TEs in their Hox clusters. My new genome-wide study reveals that this signature of speciation is indeed pronounced in Hox clusters: only the two Anolis species from amply speciating lineages exhibit unusually TE-rich Hox clusters, while a third species (Anolis auratus, black circle in figure above) follows the norm and keeps its Hox clusters relatively free from TEs. Looking in detail at genome-wide TE landscapes of these three Anolis species, I discovered that the two species with TE-rich Hox clusters had a larger population of young, more active TEs in their genomes. In addition, the inferred timing of peak activity of these TEs broadly coincided with past speciation events.
These
results suggest that – during speciation events – TEs are unusually active and
proliferate throughout the genome. As a result, even crucial regions such as Hox clusters become invaded.
Subsequently, TEs are removed from Hox
clusters by selection until a ‘healthy equilibrium’ of TE content relative to
the genome-wide TE content is reached. This equilibrium appears highly
conserved as the Hox clusters of
almost all lizards and snakes contain close to 50% of the global TE content.
This proposed model generates a number of predictions that can be tested with
genomic data from lineages with variable rates of speciation.
How then do some Anolis species cope with having their Hox clusters invaded by TEs? Clearly, the inflation of Hox clusters – increasing the distance between genes – does not disrupt the patterning of the early embryo. Genes located at one end of the cluster remain expressed early in the head of the embryo, while genes located at the other end are expressed late in the tail. However, the successive activation of Hox genes predicts that disruption, if occurring at all, should be most pronounced towards the end of the Hox clusters. I found that this indeed is the case: one out of four Hox13 genes showed aberrant expression in the two Anolis species with TE invaded Hox clusters, but this gene was expressed as ‘normal’ in other Anolis and more distantly related lizards.
Expression patterns of the posterior Hox gene HoxD13 are showing variation between species with low and high TE content in their Hox cluster: while expression in limb buds is conserved, expression in tail tissue (black arrows) is missing in species with high TE content in their Hox clusters (A. sagrei and A. carolinensis).
My study reveals that, despite being THE textbook example of our conserved developmental toolkit, Hox genes can be tinkered with. What is more, the TE invasions of Hox clusters appear to be intimately linked to diversification. Now that Anolis lizards have shown us that it can happen, perhaps they can also show us why it happens and how.
Feiner N.
2019 Evolutionary lability in Hox cluster structure and gene expression in
Anolis lizards. Evol Letters. https://doi.org/10.1002/evl3.131
Feiner N. & Wood N.J. 2019 Lizards possess the most complete tetrapod Hox gene repertoire despite pervasive structural changes in Hox clusters. Evolution & Development. 2019;21:218–228 https://doi.org/10.1111/ede.12300
Feiner N. 2016 Accumulation of transposable elements in Hox gene clusters during adaptive radiation of Anolis lizards. Proc. R. Soc. B 283: 20161555. http://dx.doi.org/10.1098/rspb.2016.1555
When you hear about a spa, you visualize a relaxing place where soft skin peeling is commonly practiced. Even if the place is human-specific, skin peeling itself has been recorded in the “animal world,” and in a way that goes beyond your imagination.
Indeed, some species of scincid and gekkonid lizards are known to lose a part of their skin during drastic regional integumentary loss (Bauer et al., 1989, 1992a, 1993; Bauer & Russell, 1992). Such loss is dependent on the bilayering of the dermis and the inherent weakness of the outer layers of the skin and is used as an antipredator strategy (such as the tail autotomy), particularly during the early stages of subjugation by the predator (Bauer et al., 1989, 1992, 1993; Bauer & Russell, 1992). Nonetheless, this practice has severe costs related to radiation exposure (particularly in diurnal species), osmoregulation and immunological integrity (Bauer & Russell, 1992).
Back to the Caribbean island of Dominica the past month, I sampled populations of Anolis cristatellus. During the routine measurement process on a big male, I was surprised to see that the lizard lost his entire skin as soon as I touched him, the muscle being nearly apparent (Fig. 1). I measured more than 2.000 anoles, and this guy was the first one to lose his skin in my hands. Did I sample a very special individual? The response is probably “no.” Within the same day, this regional integumentary loss occurred in two adult males and one adult female A. cristatellus in total. To my knowledge, such a skin loss was not observed in anoles before. Could it be an underestimated antipredator strategy in Anolis? If yes, could it be different on island vs mainland species as suggested Bauer & Russell (1992) in gekkonid lizards? The anole world has not finished to surprise us!
References:
Bauer, A.M.; Russell,
A.P.; Shadwick, R.E. 1989. Mechanical properties and morphological correlates
of fragile skin in gekkonid lizards. J. Exp. Biol. 145(79-102)
Bauer, A.M.; Russell,
A.P.; Shadwick, R.E. 1992. Skin mechanics and morphology in Sphaerodactylus
roosevelti (Reptilia: Gekkonidae). Herpetologica.
48(124-133)
Bauer, A.M.; Russell,
A.P. 1992. The evolutionary significance of regional integumentary loss in
island geckos: a complement to caudal autotomy. 4(343-358).
Bauer, A.M.; Russell,
A.P.; Shadwick, R.E. 1993. Skin mechanics and morphology of two species of Pachydactylus (Reptilia: Gekkonidae). S. Afr. Tydskr Dierk. 28(192-197)
Dr. Claire Dufour is an ecologist and evolutionary biologist; a postdoctoral fellow of Harvard University, and currently a postdoctoral fellow and teacher at the University of Montpellier, in France. Claire is interested in the dynamic interactions between sister species and their environment. Her focus is on environmental pressures – such as competing or invasive species – on the evolution of ecological, morphological, and behavioural traits of animals such as insects, mammals and reptiles. This work has led her to take a scientific interest in the two competing species of anole (tree lizards) here in Dominica; one of which is the endemic zandoli (Anolis oculatus), the other, the invasive Puerto Rican anole (Anolis cristatellus).
The endemic zandoli
For a number of years, Claire has been studying the co-existence of these two species in Dominica, how they react and behave towards each other, and how co-existing and dealing with extreme weather events such as hurricane Maria have affected behaviour and physical morphology. Her research has suggested a number of interesting outcomes that will require further study.
When the invasive species of anole arrived in the port area around Woodbridge Bay several years ago, its spread around the island was rapid, but it followed a pattern; namely the coastal road system. Claire and other scientists, such as Jacqui Eales who first recorded and studied the invasive species (see Dominica Traveller, second edition), speculate that this movement was probably caused by transportation in vehicles. The invasive anole hitched rides and occupied predominantly a coastal territory (and still does), whereas the endemic zandoli was also present in the interior where it had developed and spread over many, many years. At first, the relationship was feared to be antagonistic in nature, with the native zandoli coming under threat. Claire believes this has now changed and that the two species have settled into a form of coexistence. Moreover, she believes that the native zandoli is now doing better and is, in fact, probably the dominant species.
In order to study anoles, many environmental and morphological attributes are noted and recorded, most of which are too detailed and complex to get into here, but examples include: the location of the tree (or other structure) that the anole is inhabiting; where specifically on the tree the anole likes to hang out (trunk, branches, higher canopy, etc.); any behavioural characteristics (for example towards other anoles); and the physical attributes of the anole itself (size, weight, colour, etc.). A further experiment has been carried out to record behavioural characteristics that involves the innovative use of mimetic robots that are designed to represent both anole species. Claire presents the robots to the lizards and records their behaviour towards specific actions and signals that she is able to control remotely and unobtrusively.
Claire’s research has resulted in many interesting findings, one of which recently made headlines in the scientific community. Claire discovered that, with regard to the anoles she measured and recorded after hurricane Maria, their ability to grip with their toepads had increased by a factor of ten compared to her pre-hurricane tests. In concluding her work this year, Claire says that this attribute appears to have not only continued but has actually increased.
The likely, though unproven, explanation is that the anoles that survived the hurricane by clinging onto trees perhaps already had a strong grip compared to those that perished, and that they may have passed on this genetic trait as part of their morphological evolution. Further studies are needed and Dominica Geographic will follow Claire’s work.
Dominica is a draw for scientific researchers such as Claire because of its relatively unspoilt natural environment, its isolation as an island (it could be viewed as a very large laboratory), and its regionally and locally endemic species. One of the first things that Claire does when she comes here for her field work is engage with local people to get their views of what they have noticed about the two species of anole. Anecdotal evidence provided by local people is often an important foundation for further field research.
Invasive or local ? Can you tell the difference ?
If you are interested in recording anoles or any other aspect of natural science in Dominica, here is one fun way to get started. Download the iNaturalist app to your smartphone and start photographing and recording the plants, flowers, birds and other critters you see when you are out walking (yes, you have to get out and explore !). Think about becoming a Dominica ‘citizen scientist’ and helping to record information about the island’s natural environment, and sharing your findings with the world.
Dominica ought to be producing more of its own scientists; encouraging, educating, and financially supporting young people with the interest and the potential. Many visiting researchers are very open to engaging and sharing their work with local people but often find it difficult to do so. More could be done to provide them with the facilities they need (classroom, lab, accommodation and so on); facilities that could also be used by a home-grown scientific community.
Interactions between native Anolis carolinensis (green anoles) and invasive Anolis sagrei (brown anoles) in the United States are discussed often here on Anole Annals. Most recently, this blog featured a local news broadcast from Louisiana and newspaper article from Florida, both of which describe a pattern that is repeated across the southern United States: When brown anoles invade a habitat, green anoles begin perching higher off the ground and thus become more difficult for anole enthusiasts to find.
Why do green anoles and brown anoles tend to occupy different perch heights in areas where they co-occur? By far the most popular explanation is that these species partition space as a means of partitioning resources, namely arthropod food. In simpler terms, they are competitors. But competition itself is not always simple. To better understand and study competition, biologists often classify competition as one of two types. Species can compete directly via aggressive encounters (termed “interference competition”) or indirectly through their shared use of a limited resource (termed “exploitative competition”). We know that green and brown anoles eat similar prey, suggesting that their competition is at least partly exploitative. Do they also engage in direct interference?
In a recently published paper in Oecologia, Katherine Culbertson (Harvard ESPP ‘18, former undergrad researcher in the Losos lab) and I tested the hypothesis that interference competition between native green anoles and invasive brown anoles occurs in the field. More specifically, we wondered if an asymmetry in interference competition might contribute to the vertical displacement of green anoles by brown anoles. To test for competitive asymmetries between the species, we used a classic method in behavioral ecology: tethered intruder trials. We presented adult male intruders to previously undisturbed focal individuals of the opposite species and videotaped the interactions. Intruders were tied around the waist with string at the end of a fishing pole with enough slack to move freely. We analyzed several aspects of the behavior of the focal lizards to evaluate asymmetries in interspecific aggression between the species: how often they attacked, how often they displayed (throat fan extensions, headbobs, and pushups), how often they retreated, and in what direction they retreated. (Disclaimer: Whenever an attack occurred, we ended the trial immediately so no lizards were harmed.)
As anticipated, we found that interference competition is asymmetric in favor of brown anoles, which are more likely to display and less likely to retreat from interactions than green anoles. In line with their arboreal tendencies, male green anoles also trend toward retreating upward more often than expected by chance. Somewhat surprisingly, these asymmetries are prevalent despite the almost complete absence of physical attacks (there were only two attacks in nearly one hundred trials, both by brown anoles). All told, our results suggest that signaling between the species and avoidance behavior by green anoles resolve most potential conflicts before they escalate to combat.
Figure 2 from our paper, which displays posterior predictions for the (a) probability of display, (b) display rate, and (c) probability of retreat of male Anolis sagrei (brown anoles, “SA”) and male Anolis carolinensis (green anoles, “CA”) when presented with a male intruder of the opposite species. Brown anoles were more likely to display and less likely to retreat than green anoles.
Many Floridians I’ve met in the course of my fieldwork have described brown anoles as bullies. Although anecdotal observations of animal behavior do not always reliably represent biological truths, in this case, the collective of observations made the residents I’ve spoken with are concordant with our data. Kudos to the many local naturalists who’ve shared their stories!
In closing, I’ll attempt to refine the metaphor of brown anoles as bullies, in acknowledgement that metaphors are often imperfect and with apologies to those who bristle at any attempt to anthropomorphize non-human animals. First, what makes a bully effective? On the playground, a bully might gain a reputation as such by initiating and winning a fight. Afterward, the mere threat of physical combat is often enough for the bully to exert his or her will on others. At our study sites, where green anoles and brown anoles have co-existed for several generations, brown anoles tend to dominate interactions with green anoles without attacking them. Perhaps physical combat is more common during the incipient stages of brown anole invasion, a hypothesis which could be tested by applying our methods across sites that vary in their invasion history.
Second, what’s the best way to deal with a bully? Many children learn to ignore bullies, a strategy rendered possible by the existence of alternative space to play or activities to engage in. Green anoles appear to find refuge in the canopy, where brown anoles seldom venture. Anecdotally, areas where no such canopy exists (i.e. areas with few plants or with only short, shrubby vegetation) are the areas where green anoles are most likely to disappear entirely following brown anole invasion. This hypothesis deserves a formal test.
Special thanks to the Aquatic Preserve Program run by the Florida Department of Environmental Protection for making this work possible. Check out the paper to learn more about our methods, results, and the implications of our findings.
Katherine Culbertson marking the location of a captured green anole in the field.
Over on Biology of Mexican Herps, Levi Gray has started a new series where he examines some currently recognized Mexican Anolis to discuss whether, in fact, they are valid species. In the first installment, he discusses the case of Anolis utowanae. Check it out!
Simon Harris, a research student at the University of Gloucestershire, is seeking herpetologists to participate in a survey on the use of artificial hiding places (“refugia”).
Calling on anyone who has ever conducted a reptile survey! My name is Simon Harris, I'm a research student @uniofglos conducting a survey on the use of artificial refugia in reptle surveying. Would greatly appreciate anybody filling it out.https://t.co/aFULHhm8th
What he has in mind is the placement of artificial cover on the ground, under which reptiles might seek refuge. I’ve participated in such a study myself, using large plywood boards to sample Butler’s garter snakes (Thamnophis butleri) around Milwaukee, Wisconsin.
The method doesn’t seem that propitious for anoles. I can imagine artificial cover on walls or trees being a good technique for geckos– I’ve often surveyed house geckos using existing artificial objects (tapestries, paintings, etc.), but anoles, which were present at all sites surveyed, rarely turned up in a gecko survey. If anyone has ever used such a technique, or a similar one, for anoles, please tell us in the comments, and let us know how it worked. And, since many anologists have broader herpetological experience, if applicable, please fill out Simon’s survey!
Photo by Peter May (https://media.eurekalert.org/multimedia_prod/pub/web/191913_web.jpg?w=650)
A year ago, we mentioned reports of brown anoles (A. sagrei) in Germany, green anoles (A. carolinensis) in southern Spain and the Canary Islands (reviewed here), as well as a report of Cuban knight anoles (A. equestris) also on the Canary Islands, and asked if there were other sightings. Now we have one!
Reader Rick Wallach writes in:
I just returned to Miami from a week in Alcala de Henares near Madrid, Spain. On Tuesday night, July 9th, a colleague and I were walking through the Plaza de Cervantes at about eight PM (Spanish time) when I noticed an <i>A. sagrei</i> sitting on the rim of a cement planter displaying its dewlap. This is such a common sight to me, it took a second for it to sink in that I was not at home but in the middle of Spain. As I approached for a closer look the lizard darted into the shrubs and disappeared, but there’s no doubt about what I saw.
The question, of course, is whether the little feller was an escaped pet or indicative of yet another feral population of this ubiquitous species. I suspect the former, since during Madrid area winters the nighttime temperature drops into the mid-thirties F. Even so, I’d be curious if anyone else knows of reported sightings of brown anoles on the Iberian peninsula.
PS – I should add that even if central Spain is too cold from late October – April to support a feral population of sagrei, southern coastal Spain from Isla Cristina, around the coast past Cadiz to Gibraltar and then back northward maybe halfway to Barcelona, is much warmer and would support them handily.
Yet another newspaper article on brown anoles supplanting green anoles. This one from The Times of Apalachicola and Carabelle in Florida. The text of the article is reprinted below, but it contains maps and other figures that you’ll have to go to the original to see. Also, the article included the video above.
Cuban anoles at war with native Carolinians
By James Hargrove Special to the Times
Posted Jul 11, 2019 at 9:36 PMUpdated Jul 11, 2019 at 9:36 PM
The Forgotten Coast is being invaded by an exotic lizard called the Cuban brown anole. This may not be a crisis unless you are a native green anole, in which case, raise the alarm because the newly-arrived brown anoles really are eating your young. And once invasive brown anoles are established, there is no way of removing them.
For the past 10 years, most of the anoles in local yards were the little green natives called Carolina anoles. They are not true chameleons, but some people call them that because they can change their color from brown to green. As every child knows, the males climb up tree trunks and flower stems and flash their rosy pink throat pouches, called dewlaps, to let females know they are interested.
But this year, green anoles have become scarce. Most of the anoles in my yard are now brown to black, with a light stripe down the back, and their throat pouch is bright orange rather than pink. Some of the males also have a raised crest from head to tail like a mini-dragon. Unlike Carolina anoles, brown anoles cannot change color, so no one will mistake them for chameleons.
When brown anoles appear, green anoles take to the treetops and become scarcer. Green anoles also adapt to their new situation by becoming even better tree climbers. Scientists have shown that the foot pads on green anoles become larger over time when brown anoles force them into tree canopies. This change is said to be a case of rapid genetic adaptation going on before our eyes.
Naturally, two similar species that are competing for food and territory will fight each other. Island resident Kimberly Alexis recently took a video of green and brown anoles fighting on a fence in her yard. Although the green lizard attacked the brown one, the brown anole quickly got a good bite on the green anole’s head. It surely would have won the contest if Kimberly had not broken up the fight. (See photo)
2/2HIDE CAPTION
A 2004 map showing the range of brown anoles did not include Franklin County, but they are here now [ CaliforniaHerps.com ]
1/2HIDE CAPTION
A Cuban brown anole fights with a green anole on a fence on St. George Island [ Kimberly Alexis | Special to the Times ]
2/2HIDE CAPTION
A 2004 map showing the range of brown anoles did not include Franklin County, but they are here now [ CaliforniaHerps.com ]
1/2HIDE CAPTION
A Cuban brown anole fights with a green anole on a fence on St. George Island [ Kimberly Alexis | Special to the Times ]
2/2HIDE CAPTION
A 2004 map showing the range of brown anoles did not include Franklin County, but they are here now [ CaliforniaHerps.com ]
At first, I thought the brown anoles were merely green ones changing their color. Then a friend said, no, it is actually a different species that is creating havoc among the local lizards. It turns out that we humans accidentally imported the lizards with cargo coming from Cuba and the Bahama Islands. The brown anole first arrived on a ship that was unloaded on the Florida peninsula or the Keys around 1887 and began spreading north, (See map)
A map from 2004 that depicts the distribution of brown anoles does not show them in the Florida Panhandle, but not only are they in Franklin County, they are already on the barrier islands. Clearly, their range is expanding. How a land-loving lizard got to the barrier islands is anybody’s guess. One possibility is that they arrived as eggs in the roots of potted house plants.
Like a lot of other lizards in Florida, brown anoles are also kept as pets, and some of the feral population probably escaped into the wild. The Florida Fish and Wildlife Conservation Commission compiled a list of non-native reptiles that are now established in Florida, and they list 20 kinds of exotic anoles and their relatives that now live here.
The brown anole is hardly alone. Over 170 different reptiles have been introduced into Florida from imported cargo, from release of pets, or from zoos and research facilities after hurricanes. FWC lists 54 exotic reptiles that now have established breeding populations in the state, meaning that they have been present for 10 years. For example, Alexis mentioned that she also finds Mediterranean house geckos in her yard. Like most lizards, house geckos were brought here as pets but escaped and quickly became established.
The best known and most destructive escaped reptile in Florida is the Burmese python, which eats any native bird, mammal or even alligator it can wrap its coils around. Except for humans, mature alligators are the only animal large enough to return the favor and eat pythons.
I may be the last person in Franklin County to have noticed brown anoles, partly because there are many kinds of small lizards in the county. We have blue-tailed skinks, red skinks, Mediterranean house geckos, and legless Eastern glass lizards that many people mistake for snakes. Glass lizards have a checkered diamond pattern on their body that makes them look like a men’s tie, so my wife calls them “menswear lizards.”
From the standpoint of homeowners and gardeners, brown anoles are beneficial. Although they do eat the eggs of green anoles, they also eat flying insects, grasshoppers, spiders and even cockroaches. One can only hope that they will also dine on gnats and mosquitoes!
James Hargrove, a retired university professor who now lives on St. George Island, is a regular contributor to the Times on subjects of history and science. He can be reached atjhargrov@gmail.com
