More on the Lizard Species Whose Dewlap Differs from One Side to the Other

dewlaps

These pages have previously told the tale of Anolis lineatus, the species whose is different on one side compared to the other. Now the work has been published in Breviora. Like all publications of the Museum of Comparative Zoology, the paper can be downloaded from the museum’s publications webpage.

The research project was actually explained in a delightful video put together by the three joint authors, all of whom are headed to college this fall.

curious case

A Green Anole That’s Blue

Photo by Carissa Wickens

Photo by Carissa Wickens

Eileen Wickens, who just finished the fourth grade in north central Florida, is a lizard-catching machine and particularly adept at nabbing blue-colored green anoles (Anolis carolinensis). Here’s the story, relayed by her mom, Carissa:

The teal lizards do seem rare as we have only seen a few. We had one at our house last spring and the photo I sent you was taken at our horse teaching unit in Gainesville. We were running an equine behavior trial that day (we’re actually investigating startle phenotypes and genetics in our Quarter Horse herd), and I saw the lizard as we were packing up our gear. My daughter is very good at spotting and catching them, so we will definitely keep our eyes out and would be happy to provide a specimen for your genetic research if we can. I’ve attached the photo of the lizard we had at the house last spring. The green anoles are scare in our neighborhood and on campus compared to the brown anoles (short snouts with distinct, dorsal diamond or striped markings). They seem to far outnumber the greens. 

From our brief observations of those two blue lizards this past year it does not appear they turn the bright green you see on the other Carolina Anoles, but it would be good to observe them for a longer period of time to be certain. 

Local Adaptations and Signal Function in Sympatric Lizards

Figure 1 - Long-nosed (Gowidon longirostris) dragon performing a territorial.

Figure 1 – Long-nosed (Gowidon longirostris) dragon performing a territorial.

In the Greater Antilles, lizard radiations have produced the same suite of ecomorphs on different islands as a consequence of adaptations to similar environments. In the same way, species that use motion-based signals, and occur in sympatry, would be expected to develop similar adaptations to enhance signal efficacy as they are frequently exposed to the same environment (e.g. background noise). Additionally, sympatric species often develop mechanisms to ensure they can distinguish between conspecifics and heterospecifics, particularly if they are closely related. This means that potentially opposing selective pressures might be at work for such systems.

Agamid lizards are widespread across the Australian mainland, and species distributions regularly overlap, especially in arid and rocky habitats. We analysed the motion-based signals of two pairs of sympatric species of Australian agamids to consider how they maintain reliable communication, while at the same time they avoid misidentification during signalling interactions. We calculated the speed distributions of the motion produced by lizard signals, and also by the environment (i.e. background noise). We then compared these two sources of motion to obtain a measure of signal-noise contrast, which indicates how much the signals stand out from the background and is therefore a proxy for signal efficacy (see Ramos & Peters 2017a).

The ring-tailed dragon (Ctenophorus caudicinctus) and the long-nosed dragon (Gowidon longirostris; Figure 1) are often found in sympatry in south Northern Territory and southeast Western Australia, around gorges and rocky outcrops. We recorded territorial displays at West MacDonnell National Park, in Northern Territory. The two species differed in display complexity (example of displays by all four species) and motor pattern use, as well as overall morphology (Figure 2). Interestingly, the speeds produced during their displays (Figure 3) and their signal-noise contrast scores were strikingly similar. Not only that, but their scores indicate that the signals from both species are highly effective in the context of the plant environment. These results demonstrate similar adaptations to their shared environment, while maintaining species recognition cues through morphology and overall display appearance.

The core motor patterns refer to HB = head bob, LW = limb wave, PU = push up, TC = tail coil, and TF = tail flick (Ramos and Peters 2016). Ctenophorus caudicinctus has been observed performing limb waves, but this motor pattern is not present during its territorial displays. (Figure adapted from Ramos & Peters 2017 Journal of Comparative Physiology A)

Figure 2 – Habitat, average snout-vent length and known repertoire of core motor patterns for both species pairs. The core motor patterns refer to HB = head bob, LW = limb wave, PU = push up, TC = tail coil, and TF = tail flick. Ctenophorus caudicinctus has been observed performing limb waves, but this motor pattern is not present during its territorial displays. (Figure adapted from Ramos & Peters 2017 Journal of Comparative Physiology A)

The military mallee dragon (Ctenophorus fordi) and the painted dragon (Ctenophorus pictus) are very common in arid and semiarid sandy areas of northwest Victoria, South Australia, and southwest Queensland. We recorded displays at Ngarkat Conservation Park in South Australia, where they are often found in sympatry. These two species are much closer in appearance, but their display complexity and motor pattern use were just as contrasting as in the previous pair of lizards (Figure 2). In addition, the speeds produced during their displays and their signal-noise contrast scores were considerably higher in the painted dragon (Figure 3). We suggest this difference is related to the lack of territoriality in mallee dragons. This species is not known to protect territories or perform aggressive displays, so the motivation to produce conspicuous signals is likely to be reduced compare to its territorial relatives.

Figure 2 - Comparisons of the motion speed distributions for all species. Kernel density functions for a) Ctenophorus caudicinctus (red) and Gowidon longirostris (black), and b) C. fordi (red) and C. pictus (black), averaged within species. (Figure adapted from Ramos & Peters 2017 Journal of Comparative Physiology A)

Figure 3 – Comparisons of the motion speed distributions for all species. Kernel density functions for a) Ctenophorus caudicinctus (red) and Gowidon longirostris (black), and b) C. fordi (red) and C. pictus (black), averaged within species. (Figure adapted from Ramos & Peters 2017 Journal of Comparative Physiology A)

In this study we were able to show that the ring-tailed and long-nosed dragon perform displays with almost identical motion speed distributions and signal-noise contrast scores, despite utilising very different territorial displays (see Ramos & Peters 2017b for more details). In the case of the other sympatric pair, motion speed distributions and signal-noise contrast scores appeared to be much higher in the painted dragon than in the non-territorial mallee dragon. This difference in social behaviour could be key to explaining why the signals of the sympatric C. caudicinctus and G. longirostris seem equally well adapted to their local environmental noise, as evidenced by their equally high signal-noise contrast scores, but the signals produced by C. fordi and C. pictus do not. Thus, the selective pressure to generate signals with high efficacy appears to be mediated by signal function, at least in this context.

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Where Are All the Green Anoles?

For the past eight years, my lab has conducted intensive research on green anoles (Anolis carolinensis) in Palmetto State Park in Luling, Texas, about an hour east of San Antonio. This park is beautiful – it’s centered around a swampy area dominated by dwarf palmettos (Sabal minor), and the San Marcos River flows through it. We’ve marked lizards and mapped their home ranges, watched their behavior, measured their morphology and parasite loads, and so much more. In past years, we’ve calculated that the density of green anoles in the park is approximately 0.04 lizards/m2, or about four adult lizards in every 10m x 10m area. We could regularly get sample sizes of around 150 lizards for behavioral studies in the park, but we very rarely collected animals from the park – we left them where we found them!

But this year is different. On three field trips to the park this summer, we have found very few green anoles. On our first visit this year in May, we spent 16 person-hours searching for lizards and found four green anoles. On our second visit in early June, we spent 14 person-hours searching and found eight. Last week, we spent another 12 person-hours and found only two. We see green anoles all over the city of San Antonio, and the students in my team are all skilled lizard spotters and catchers, so this isn’t due to inexperience. Also, we see other species of lizards all over the park – most commonly, Texas spiny lizards, little brown skinks, and house geckos– as well as garter snakes, copperheads, and cottonmouths. We also see tons of frogs.

Garter snake eating a tree frog, at Palmetto State Park. Other herps are thriving there!

Garter snake eating a tree frog, at Palmetto State Park. Other herps are thriving there!

So what happened to the anoles? We’ve considered a number of possibilities. The first thing we thought of was the possibility of feral cats – but we haven’t seen any cats in the park, and we think cats should have the same effect on the other herp species. What if the insect population had crashed? But again, that would affect the other lizards, snakes, and frogs too. This isn’t a year of particular drought or excess rain (and in previous wet and dry years, we’ve still seen lots of anoles), and the vegetation throughout the park largely looks the same as it has in the past. Perhaps an anole-specific disease has spread through this population?

In any case, the paucity of anoles in the park this year suggests that there won’t be many next year either, as there’s almost no one around laying eggs. It’s a bummer, because we’ve had such success here in the past.

Any ideas to explain this, AA readers?

 

Work we’ve published from our previous research in Palmetto State Park:

  • Dill, A.K., T.J. Sanger, A.C. Battles and M.A. Johnson. 2013. Sexual dimorphisms in habitat-specific morphology and behavior in the green anole lizard. Journal of Zoology 290: 135-142.
  • Battles, A.C., T.K. Whittle, C.M. Stehle, and M.A. Johnson. 2013. Effects of human land use on prey availability and body condition in the green anole lizard, Anolis carolinensis. Herpetological Conservation and Biology 8: 16-26.
  • Bush, J.M., M.M. Quinn, E.C. Balreira, and M.A. Johnson. 2016. How do lizards determine dominance? Applying ranking algorithms to animal social behavior. Animal Behaviour 118: 65-74.
  • Stehle, C.M., A.C. Battles, M.N. Sparks, and M.A. Johnson. In revision. Prey availability affects territory size, but not territorial display behavior, in green anole lizards. Acta Oecologica.

Evolution 2017: Anoles and Ameivas Have Similar Gut Microbiomes

Late Breaking: one last Evolution 2017 post!  Last weekend during the Evolution meeting, I had a chance to chat with Iris Holmes (Ph.D. student, University of Michigan) about the poster she presented. Initially not on our watch list because of the lack of “anole” in the description, my eye caught the dewlapping lizard perched at the top of her poster from across the room.

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Iris presented her work on gut microbiomes of two groups of lizards: anoles and ameivas. She wanted to know if different taxa have different gut microbiomes and to what extent diet influences bacterial composition of gut microbiomes. Her collaborator (Ivan Monagan) collected scat samples from 22 Anolis dollfusianus and 9 Ameiva from an agricultural area in the Soconosco region of Chiapas, Mexico. Together, they then sequenced both the gut bacteria and the digesting prey with two 16S primers. Iris chose to target the prey as well because she wanted to know if they were eating different things and how different stages of digestion influence gut bacteria communities.

Iris found that there were no clear differences between the gut microbiomes of anoles and ameivas. Both species had gut microbiomes dominated by three main phyla: Proteobacteria, Firmicutes, and Bacteroidetes. Little is currently known about how these bacteria relate to digestion and health in reptiles, but Iris commented that we can make some guesses based on studies in other taxa. Proteobacteria are a disease indicator in mammals, but appear to be normal in reptiles and birds. Firmicutes and Bacteroidetes are both important for digestion of carbohydrates and fats (respectively) in mammals. Iris found that there was a loose correlation between the amount of prey consumed and the abundance of Bacteroidetes, suggesting these bacteria also play a role in digestion in lizards. She also found that there was an apparent tradeoff between the Proteobacteria and the two other groups – sequence abundance of proteobacteria was negatively correlated with abundance of Bacteroidetes and Firmicutes. Overall, this is an interesting first step in understanding the gut microbiomes of reptiles and how they differ (or don’t) between groups.

Metabolism Rate Data on Anoles?

I’m hoping that some of you out there have been collecting Basal Metabolic Rate or Resting Metabolic Rate data on Caribbean anoles!

I’m working with a group of scientists on a large-scale comparative database on circulating hormones in free-living vertebrates – we call our collaboration HormoneBase – and we’re hoping to look at relationships between hormone levels and metabolism. (We’ll be presenting some of this work at the Society of Integrative and Comparative Biology meeting in January 2018 – check out our symposium announcement here!) We have a good list of anole species in the database, thanks to the work of Jerry Husak and Matt Lovern (2014), but it seems that very little metabolism rate data are available for these species. Do you know of such data, or do you have them – published or unpublished? If so, please contact me (mjohnso9@trinity.edu)!

 

Reference:

Husak JF and MB Lovern. 2014. Variation in steroid hormone levels among Caribbean Anolis lizards: endocrine system convergence? Hormones and Behavior 65:408-415.

Subfossil Record Reveals Human Impacts on a Lesser Antillean Endemic Anole

Figure 2: Landmarks (black point circled in white) and sliding landmarks (black points) used in the geometric morphometric analysis.

Figure 1. Landmarks (black point circled in white) and sliding landmarks (black points) used in the geometric morphometric analysis.

The knowledge of the past squamate fauna of the Guadeloupe islands (French Lesser Antilles) dramatically increased these last years in the framework of two European paleontological research programs. New archaeological and paleontological excavations (about which I previously talked) have been conducted and led to the discovery of thousands of squamate remains allowing to complete the pioneering works conducted by G. K. Pregill in the 90’s (Pregill et al., 1994). Results obtained on iguanas (Bochaton et al., 2016b), galliwasps (Bochaton et al., 2016a), ameivas (Bochaton et al., 2017a) and other taxa (Bailon et al., 2015; Bochaton et al., 2015; Boudadi-Maligne et al., 2016) point to high extirpation and extinction rates, mainly taking place during the last centuries after the European colonization of the archipelago and probably in relation to introduction of exogenous competitors and predators, as well as the practice of intensive agriculture.

In the middle of all of these extinctions, anoles, which are still very common in Guadeloupe, appeared to be kind of indestructible and were apparently not impacted at all by recent anthropogenic disturbances. However, the study of a huge assemblage of anole remains from Marie-Galante Island dated from Late Pleistocene to the 14th century reveals that this first impression was far from true.

Nearly 30,000 anole remains coming from several deposits were investigated using a combination of morphological and morphometric approaches. Size estimations (see Bochaton, 2016; Bochaton and Kemp, 2017) indicate that whatever the stratigraphic layer they come from, fully mature individuals range in three groups of Snout-Vent Length (SVL) size (Figure 2).

Figure 2.  SVL reconstructed on the basis of fully mature humeri (N = 66) with the results of a mixture analysis indicating a trimodal distribution. MTMS1, minimal theoretical maximal size obtained from the smallest fully mature humerus; MTMS 2, minimal theoretical maximal size obtained from the largest immature humerus; MTMS 3, minimal theoretical maximal size obtained from the smallest mature humerus included in the intermediately sized group.

Figure 2. SVL reconstructed on the basis of fully mature humeri (N = 66) with the results of a mixture analysis indicating a trimodal distribution. MTMS1, minimal theoretical maximal size obtained from the smallest fully mature humerus; MTMS 2, minimal theoretical maximal size obtained from the largest immature humerus; MTMS 3, minimal theoretical maximal size obtained from the smallest mature humerus included in the intermediately sized group.

These SVLs partly match those of the females (max 75mm SVL) and males (max 120 mm SVL) of the modern solitary Marie-Galante anole (Anolis ferreus). However, a third group of fossil specimens of very large size reaching 150mm SVL also occurred in the deposits and has no modern counterpart on the island. Still, morphological analysis indicates that these large specimens were also A. ferreus. A geometric morphometric analysis (Figure 1, above) was also conducted on dentaries of Marie-Galant fossils and included in a modern sample of Lesser Antillean anoles.
Figure 3. Two first axes of the PCA conducted on shape data collected for fossil and modern A. ferreus dentaries showing a diminution of morphological variability between fossil and modern anoles.

Figure 3. Two first axes of the PCA conducted on shape data collected for fossil and modern A. ferreus dentaries showing a diminution of morphological variability between fossil and modern anoles.

This analysis reveals a strong heterogeneity of the morphology of the dentary mostly depending of their size (allometry). The three fossil size groups are however closer to modern A. ferreus than to any other modern taxa and are linked by a common allometric relationship between their size and shape which differs from modern A. ferreus. The morphological variability of the fossil dentaries is also higher than that of modern A. ferreus (Figure 3).

These results indicate that all fossils are likely to correspond to A. ferreus. However, fossil representatives are more morphologically variable in terms of size, shape, and allometry than modern A. ferreus.The morphology of fossil A. ferreus remained stable during more than 30,000 years before an abrupt change that occurred during the last centuries. There is, however, a void of fossil data during the modern period which precludes linking this reduction of morphological variability between fossil and modern A. ferreus to a distinct event. Yet, this phenomenon is contemporaneous to the numerous extinction events documented on Marie-Galante and is thus very likely to be also related to the anthropization of the island.

This study also provides a strong argument again the hypothesis of the past occurrence of a second anole species smaller than modern A. ferreus on Marie-Galante and used to explain the large size reached nowadays by this insular solitary anole.

More details can be found in the publication of this work:

Bochaton, C., S. Bailon, A. Herrel, S. Grouard, I. Ineich, A. Tresset, and R. Cornette. 2017b. Human impacts reduce morphological diversity in an insular species of lizard. Proc. R. Soc. B 284:20170921.

References

Bailon, S., C. Bochaton, and A. Lenoble. 2015. New data on Pleistocene and Holocene herpetofauna of Marie-Galante (Blanchard Cave, Guadeloupe Islands, French West Indies): Insular faunal turnover and human impact. Quaternary Science Reviews 128:127–137.

Bochaton, C. 2016. Describing archaeological Iguana Laurenti, 1768 (Squamata: Iguanidae) populations: size and skeletal maturity. International Journal of Osteoarchaeology 26:716–724.

Bochaton, C., and M. E. Kemp. 2017. Reconstructing the body sizes of Quaternary lizards using Pholidoscelis Fitzinger, 1843 and Anolis Daudin, 1802 as case studies. Journal of Vertebrate Paleontology 37:e1239626.

Bochaton, C., R. Boistel, F. Cassagrande, S. Grouard, and S. Bailon. 2016a. A fossil Diploglossus (Squamata, Anguidae) lizard from Basse-Terre and Grande-Terre islands (Guadeloupe, French West-Indies). Scientific Report 28475:1–12.

Bochaton, C., S. Grouard, R. Cornette, I. Ineich, A. Tresset, and S. Bailon. 2015. Fossil and subfossil herpetofauna from Cadet 2 Cave (Marie-Galante, Guadeloupe Islands, F. W. I.): Evolution of an insular herpetofauna since the Late Pleistocene. Comptes Rendus Palévol 14:101–110.

Bochaton, C., S. Bailon, I. Ineich, M. Breuil, A. Tresset, and S. Grouard. 2016b. From a thriving past to an uncertain future: Zooarchaeological evidence of two millennia of human impact on a large emblematic lizard (Iguana delicatissima) on the Guadeloupe Islands (French West Indies). Quaternary Science Reviews 150:172–183.

Bochaton, C., R. Boistel, S. Grouard, I. Ineich, A. Tresset, and S. Bailon. 2017a. Evolution, diversity and interactions with past human populations of recently extinct Pholidoscelis lizards (Squamata: Teiidae) from the Guadeloupe Islands (French West-Indies). Historical Biology.

Boudadi-Maligne, M., S. Bailon, C. Bochaton, F. Cassagrande, S. Grouard, N. Serrand, and A. Lenoble. 2016. Evidence for historical human-induced extinctions of vertebrate species on La Désirade (French West Indies). Quaternary Research 85:54–65.

Pregill, G. K., D. W. Steadman, and D. R. Watters. 1994. Late Quaternary vertebrate faunas of the Lesser Antilles: historical components of Caribbean biogeography. Bulletin of Carnegie Museum of Natural History 30:1–51.

Evolution 2017: Thermoregulation Simultaneously Impedes and Impels Evolution

Major Anole Annals contributor Martha Muñoz gave a brilliant talk at the Evolution meeting  as an awardee of a well-deserved ‘Young Investigator’ award from the American Society of Naturalists. In her talk, Muñoz discussed how two classic papers by Janzen (1967) and Huey et al. (2003) influenced the way she thinks about the interplay between behavior, physiology, and evolution. Not surprisingly, Anolis lizards played a leading role in her exposition.

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Martha Muñoz introduces the Cybotoid Anoles.

Martha’s talk, entitled “Janzen’s hypothesis meets the Bogert effect: a synthesis nearly 100 years in the making”, started by describing Janzen’s hypothesis. In short, Janzen (1967) predicted that physiological differences among populations across altitudinal bands would be stronger in tropical mountains than in temperate ones. The main argument was that populations can more easily adapt to a given temperature range in tropical environments because these ranges are stable throughout the year, whereas the temperatures of different altitudinal bands overlap more in temperate areas due to seasonal variation.

Martha explains how daytime and nighttime temperatures in the tropics mirror seasonal patterns in temperate and tropical climates.

Martha explains how day and night temperatures in the tropics mirror seasonal patterns in temperate and tropical climates.

Expanding on Janzen’s idea, Muñoz hypothesized that diurnal and nocturnal temperature variation in a single tropical mountain could also generate differences in physiological divergence among lowland and highland populations. The idea was that daytime temperatures were variable with overlap across elevation (similar to the seasonal picture in temperate areas) and nighttime temperatures were more constant and differed between elevations (similar to the seasonal picture in tropical areas).

To test this, Martha sampled populations in the Dominican Republic at sites ranging in elevation from sea level to 2400m. She then analyzed heat and cold tolerance of several species of anoles from the Anolis cybotes group. Results on cold tolerance (CT min) seem to agree with Janzen’s hypothesis: cold tolerance strongly covaries with altitude at night, with higher elevation populations having lower critical thermal minimums. Interestingly, however, heat tolerance (measured as CT max) was not at all associated with elevation.

Why did Janzen’s hypothesis fail to explain the evolution of heat tolerance across the altitudinal range? This question led to a key point of Muñoz’s talk: Janzen’s hypothesis might fail to predict evolution of CT max because it is agnostic about behavior. In the case of ‘cybotoid’ anoles, lizards from different altitudes could actively adjust their habitat use to achieve optimal temperatures. As a consequence, thermoregulatory behavior could forestall evolution of physiology in heat tolerance. By studying habitat use across different elevations, Muñoz showed that, although anoles behave as thermo-conformers at low elevations, they clearly thermoregulate at high elevations. In other words, anoles were at similar temperatures to the average available substrates in lowlands but their body temperatures were significantly higher than perches at higher elevation.

Martha explains how the thermoregulation can lead to slower evolution in a trait (the Bogert effect)

Martha explains how the thermoregulation can lead to slower evolution in a trait (the Bogert effect)

This was at least partially explained by habitat use differences: anoles at high elevations perched most frequently on boulders, which are on average about 5º C warmer than trees –the most used substrate in low altitudes. In fact, 90% of the trees Martha sampled at these high elevation sites were lower in temperature than the preferred temperature of the lizards! These data indicate that anoles from the A. cybotes group have buffered natural selection in physiology by means of behavioral adjustments –a phenomenon known as the Bogert effect (also called behavioral inertia; Bogert 1949).

Finally, the talk had a third part. And yes, it got even more interesting! Due to the observed habitat use differences in high latitudes, Muñoz and her collaborators predicted that although behavior could buffer physiological evolution on heat tolerance, it could spur evolutionary change in ecologically-relevant morphological traits (the behavioral drive hypothesis). Specifically, they predicted that increased use of boulders (for thermoregulation) at high elevations should drive morphological shifts in traits related to boulder use: head and limb morphology. They found evidence for these hypothesized morphological differences: high elevation lizards had higher head heights and longer hindlimb,  in agreement with functional predictions. Finally, a captive breeding experiment confirmed that these differences were the consequence of genetic changes and not simply due to developmental plasticity.

Martha’s research is a great example of how, as Huey said, studying behavior can be crucial to improve our understanding of evolutionary processes. We are looking forward to hear about future research from the Muñoz lab, which is about to open at Virginia Tech!

 

References:
Janzen, D.H. 1967. Why mountain passes are higher in the tropics. American Naturalist 101:233–249

Huey, R.B., Hertz, P.E., Sinervo, B. 2003. Behavioral drive versus behavioral inertia in evolution: a null model approach. American Naturalist 161: 357–366.

Muñoz, M.M. et al. 2014b. Evolutionary stasis and lability in thermal physiology in a group of tropical lizards. Proc. R. Soc. B 281: 20132433.

Muñoz, M.M., Losos, J.B. Thermoregulation simultaneously promotes and forestalls evolution in a tropical lizard. (Accepted pending minor revision). American Naturalist.

Evolution 2017: Spatial Structuring of Urban Green Anoles

In his Masters thesis conducted in Simon Lailvaux’s lab at the University of New Orleans and presented this week at Evolution 2017, David Weber used a multiyear data set of Anolis carolinensis lizards’ locations and morphology as well as a DNA-based pedigree to investigate the effects of body size and relatedness on the spatial distribution of these lizards. Specifically, he set out to test three hypotheses: first, are males’ home ranges larger than females’ home ranges? Second, are bigger males more likely to be surrounded by smaller males that are related to them? And third, is there any evidence for the inheritance of home ranges from parent to offspring?

Anolis carolinensis dewlapping. Photo by Cowenby available on Wikipedia.

Anolis carolinensis dewlapping. Photo by Cowenby available on Wikipedia.

Lizard locations were sampled in an urban New Orleans park twice a year, in the fall and in the spring, from 2010 to 2015. The dataset included over 800 individuals, and what struck me most about these data was that, of these 800+ individuals, fewer than 100 were observed often enough to estimate home range volumes–death and dispersal can rule these lizards’ lives! Male and female home range volumes did not differ significantly (and the trend was in the direction of females moving over larger areas, which concurs with data from Robert Gordon’s 1956 thesis on green anoles, but with little else, I think). Curiously, smaller neighbours of the biggest males were less related to them than were males found farther away, suggesting that male anoles don’t preferentially tolerate their kin over non-kin. And though philopatry  (aka site fidelity aka staying the same place) was rare overall, females were a bit more likely to co-occur with their male offspring than males were. In a result that conforms to traditional wisdom, Weber found that the biggest males in the site seemed to avoid each other, potentially spacing themselves as far apart as possible.

Following a kind shout-out to my and Jonathan Losos’ recent paper on Anolis territoriality or the lack thereof, Weber chose to interpret his results as making sense only outside of a territorial framework. Unsurprisingly, I concur with this decision entirely, and am excited to see where Weber goes with this idea in the publications resulting from this mammoth dataset!

Evolution 2017: Integrating Ecological, Antagonistic and Reproductive Character Displacement

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The arrival of an outsider that overlaps in resource use and habitat with local species can lead to intense competition between the two. A result of this competition can be character displacement, where traits of the species (one or both) change in sympatric populations (where the co-occur), but not in allopatric populations. Claire Dufour (Post-Doctoral researcher at Harvard University) presented her work on character displacement for two anole species on the island of  Dominica: the native Anolis oculatus and the introduced Anolis cristatellus. Her objective was to integrate ecological, antagonistic and reproductive character displacement. Specifically, she tested whether competition  between these new island-mates leads to changes in habitat use, morphology, and display behavior.

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Location of populations of the introduced A. cristatellus with the sampled area, Calibishie inset

Claire compared allopatric populations of the two species with sympatric populations in the northern area of the island in Calibishie, where Anolis cristatellus has been present for two years. She found that in sympatry, both morphological and behavioral shifts have occurred. In sympatry, Anolis oculatus perched higher and had shorter limbs. She also found differences in display behavior, which she tested with an anole robot programmed to dewlap and do push-ups. This experiment showed that in sympatry, Anolis cristatellus dewlapped less, but Anolis oculatus does not alter its display behavior. Future work will test for reproductive character displacement and contrast populations where Anolis cristatellus has been present for a longer time span.

Evolution 2017: Sensory Drive and Lizard Adaptive Radiation

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The Sensory Drive hypothesis predicts that species will evolve communication signals that are effective in the particular light environment in which they occur. Anolis lizards are an excellent example: in dark habitats, they tend to have light-colored, highly reflective (and transmissive) dewlaps that are usually yellow or white in color, whereas in bright, open environs, dewlaps tend toward blue, black, orange or red. However, demonstrating that these dewlaps are actually effective at being visible in their particular habitats has proven surprisingly challenging.

Leo Fleishman has been a leader in this area and in a talk at the sensory ecology symposium at the evolution meetings, he presented new and exciting developments. First, in line with previous work, he showed that the spectral reflectance/transmittance of dewlaps is not particularly well-matched to that of the background. Rather, the same colored dewlaps appear to be maximally contrasting with the radiance of the background across all habitats:  basically all habitats have mostly green backgrounds, and red or orange stands out the best against the green background, no matter what the habitat.  So much for sensory drive, it would seem!

But more recent work saves the day: it turns out that habitats differ in the total intensity of light (number of photons coming down) they receive and that, furthermore, across species, dewlap intensity (total photons reflected and/or transmitted) is negatively related to habitat intensity (with one notable outlier, the enigmatic A. gundlachi). Under the relatively low light conditions of forest shade or partial shade, color discrimination becomes more difficult, and colors such as red and orange and other dark colors do not stand out well against the background, because they simply do not emit enough photons to efficiently drive color vision.  Yellow or white works better. Conversely, in intense light environments, there is enough light to easily see the darker colors, and these stand out well against the green background. Moreover, behavioral experiments confirm that in bright light conditions red stimuli are most visible against a green background, whereas in low light yellow stimuli are more visible.  Thus, even though most Anolis habitats have similar spectral properties, differences in total light intensity strongly influence what colors are most effective, and thus appear to have played a major role in the shaping the evolution of dewlap colors.

Leo Fleishman discusses color space in 4-dimensions, corresponding to the four cones in the anole eye. For each species, red dots are color of the dewlap and green dots are the color of the background, indicating that dewlaps stand out against their background.

Leo Fleishman discusses color space in four dimensions, corresponding to the four cones in the anole eye. For each species, red dots are color of the dewlap and green dots are the color of the background, indicating that dewlaps stand out against their background.

Evolution 2017: Introduced Miami Anoles Exhibit Character Displacement

Bright and early on the last day of the annual Evolution meeting, James Stroud (Florida International University) presented his work on character displacement in novel communities of introduced anoles in Miami. In this elegant use of a natural experiment, James looked at the novel co-existence of two anoles in their introduced range and wondered if character displacement was occurring as predicted when two ecologically similar species are found in sympatry. Specifically, James wanted to know if Anolis cristatellus and Anolis sagrei would shift their habitat use when in sympatry, resulting in correlated shifts in morphology. These species are both trunk-ground anoles of roughly the same body size. They are native to Cuba/Bahamas and Puerto Rico (respectively) and are diverged by ~50 million years.

James hypothesized that in their introduced range in Florida, these two species would diverge ecologically in sympatry but be more similar in allopatry. He found that in allopatry, both species attained similar relative abundances and perched at similar heights. However, in sympatry, both decline in relative abundance suggesting that these species are interacting strongly with one another. Even more interesting, in sympatry A. sagrei perches lower and spends more time on the ground than it does in allopatry, while A. cristatellus perches higher!

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Next James hypothesized that these ecological shifts could lead to shifts in morphology. If A. sagrei is spending more time on the ground, perhaps longer limbs would be favored. Similarly, if A. cristatellus is spending more time higher up in the trees, perhaps there would be selection for stickier toepads. As predicted, A. sagrei had longer forelimbs and hindlimbs in sympatry. However, he did not find any difference in toepad morphology between sympatric and allopatric populations of A. cristatellus. Instead, he observed that A. cristatellus in sympatry with A. sagrei had significantly smaller heads.

James ended by wondering if alternative behavioral and social mechanisms may drive these observed shifts in head morphology. Either way, this case study provides an interesting insight into how a complex range of adaptive responses can result from a seemingly simple ecological interaction.

Evolution 2017: Experimentally Testing Perch Choice in Urban and Forest Lizards

Cities and urban areas are expanding rapidly around the world, altering the environment and creating very different ecological and selective pressures for organisms that live in urban habitats. A few of the most striking differences between urban and natural habitats are higher temperatures and a huge increase in artificial substrates like the walls of buildings. These artificial substrates (e.g., metal, concrete) are not only significantly smoother than natural (i.e., trees) substrates, but also absorb, retain, and radiate heat differently. Consequently, organisms may alter their behavior to better deal with these and other challenges of city life. Since anoles cannot internally regulate their temperature, behavioral shifts may be driven by perch substrate properties, temperature, or some interaction of the two.

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Kevin Aviles-Rodriguez (U. Mass. Boston) addressed this question in urban Anolis cristatellus in San Juan, Puerto Rico. He created experimental enclosures in which each wall was a different substrate: wood, plastic, painted cement, and metal. He placed individual lizards into the enclosures and observed which wall they were perched on throughout the day. He also recorded the temperature of each wall, to determine how perch temperature of each substrate type influenced perch choice. Aviles-Rodriguez conducted this experiment in both urban and forest populations, and predicted that urban lizards would use artificial substrates more readily than forest lizards.

Interestingly, he did not find that to be the case – lizards from both urban and forest habitats used bark much more than any other surface. However, when lizards did use artificial substrates, they tended to use metal and cement when these perches were cooler, suggesting that perch temperature is a factor in perch choice. Aviles-Rodriguez plans to test these hypotheses more thoroughly by conducting additional experiments across more urban replicates to see if the same pattern emerges. He also plans to experimentally control the temperatures of different perch substrates in his enclosures to see whether lizard choices are primarily driven by perch substrate or temperature.

Evolution 2017: What Jumping Genes Can Tell Us about Anole Genome Evolution

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I find Transposable Elements (TEs) to be some of the most fascinating features of genomes. Also known as selfish genetic elements, these sequences contain the genetic machinery to create copies of themselves and insert these new copies in locations throughout the genome. The genomes of different organisms vary widely in their degree TE abundance. For example, 20% of the human genome is composed of just one kind of TE!

This morning Robert Ruggiero, a Postdoctoral Fellow in the lab of Stephane Boissinot at NYU Abu Dhabi, presented his work on the population genomics of TEs in the genomes of Anolis carolinensis populations. Robert employed a clever approach that uses a feature of next-generation sequence data to identify TE insertions. In this way, he can characterize all of the TE insertions in an individual’s genome and determine what portion of a population contains any particular insertion.

It’s easy to see how Transposable Elements could be bad for an organism. If a TE inserts itself into the middle of an important gene, the function of that gene could be interrupted, and render the bearer of that insertion less evolutionarily fit. The ability of natural selection to purge this type of deleterious insertion is governed in part by the effective population size of the group where that insertion arises. In essence, natural selection is more effective in larger populations.

Using the information he collected on TE insertions in anole populations, Ruggiero created a population genetic summary called an Allele Frequency Spectrum, the count of insertions that exist at a particular frequency in a population. This distribution can then be used to infer how well populations control the frequency of TE insertions, and in addition, estimate the effective size of those populations. Robert found TE insertions in Floridian populations of Anolis carolinensis were maintained at lower frequencies than other populations suggesting that selection is better able to purge deleterious insertions in the Florida population. He also found that different families of TEs appear to employ strategies that mirror ecological r/K theory. Some TEs create insertions frequently but few of these insertions get to high frequency, whereas other TEs insert infrequently, but those insertions that do occur are more likely to reach high frequency. Moving forward, using this line of inquiry in anoles will be an excellent opportunity to understand the control and evolutionary consequences of TEs, particularly as more Anolis genomes come online allowing comparative analyses.

Evolution 2017: Genetics of Ecologically Divergent Anoles

Anolis distichus is well-known in the anole world for the high degree of ecomorphological variation within the species, especially in dewlap color. In fact, there are 18 described subspecies! While there is some gene flow between various subspecies and populations, the phenotypic differences are maintained, which suggests strong selection. But the fine-scale genetic structure underlying these traits is not well understood. Anthony Geneva and colleagues decided to explore the genomic basis of adaptive divergence in a well-described hybrid zone between two A. distichus subspecies. The first, A. d. ignigularus, has a white dewlap, and occupies a dry forest habitat while the second, A. d. ravitergum, has a red dewlap and inhabits a wetter habitat. The two subspecies occur along a transect from dry to wet, and they hybridize in a narrow contact zone in the middle. These two subspecies provide a great system to explore the link between adaptive and genetic divergence.

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Anolis distichus. Photo by Rich Glor

Geneva sequenced individuals using RNASeq across an environmental transect from wet to dry, including allopatric and sympatric populations of both species. He examined levels of divergence and introgression to explore which genomic loci might be the basis for the ecological adaptive divergence between these two species. He found a suite of candidate genes that differ between the two subspecies, as well as several that show signs of introgression between the two. Interestingly, several of the divergent genes are involved in two traits that likely are impacted the environment – insulin signaling, which may relate to metabolic differences between hot and cool climates, and vision, which may relate to differences in light availability and signal efficiency. Most of the introgressed genes, on the other hand, relate to conserved pathways, suggesting that these genes play similar roles in both subspecies.

Adpative divergence in anoles has been a topic of interest for a long time, and Geneva’s study provides and a valuable insight to the genetic basis of this interesting phenomenon.

Evolution 2017: Does Molecular Convergence Underly Ecomorph Convergence?

2017-06-25 16.15.01On each of the Greater Antillean islands, habitat-specialist Anolis ecomorphs have independently evolved complex suites of shared phenotypes and behaviors. This remarkable convergence has motivated the work of generations of anolologists. With anoles entering the once-exclusive club of genome-enabled organisms, a new line of investigation has become possible: Is the convergence observed in anole ecomorphs caused by molecular convergence? Such convergence can take many forms, including shared changed at individuals sites, or shared changes in the rates of protein evolution of individual genes.

Russ Corbett-Detig of UCSC sought to answer this question using whole-genome sequence data from 12 species – four from each of the Trunk-Ground, Trunk-Crown, and Grass-Bush ecomorphs drawn from different islands and different evolutionary lineages. Accurately detecting molecular convergence is fraught and much recent research has focused on avoiding pitfalls that could lead to a positively misleading inference of convergence where none actually exists. Previous studies have trumpeted amazing cases of molecular convergence in a variety of animals, only to be later shown to be artifacts of data analysis.

Corbett-Detig did everything right. He used null models that account for the expected background levels of convergence caused by processes other than natural selection. He found no evidence of extra shared non-synonymous mutations in any of the three ecomorph groups. Similarly, he found no signal of shared changed in protein evolution in Trunk-Ground or Trunk-Crown but Grass-Bush anoles seemed to share elevated rates of changes in many genes. This result was exciting, but Corbett-Detig dug deeper and discovered a new way this type of analysis could be mislead – two of the four Grass-Bush anoles exhibited accelerated evolution across their entire genomes and, as a result, seemed to share faster rates at more genes than expected by chance. When Corbett-Detig corrected for this bias, the signal of convergence disappeared.

While this result was in one sense disappointing, it is also fascinating and suggests the evolutionary pathways to shared ecomorphological traits are numerous and strongly influenced by contingency. Furthermore, anole ecomorphs have evolved such a stunning set of similarities that other forms of convergence like genome structure, gene family expansion, or convergence in gene regulation may still hold the key to understanding the genetic basis the remarkable convergence of Anolis ecomorph classes.

Evolution 2017: Sexually Antagonistic Selection in Juvenile and Adult Anoles

Sexually antagonistic selection occurs when traits are beneficial for one sex, but detrimental to the other. This commonly occurs in species with sexual dimorphism, such that one trait is positively correlated with fitness in one sex, and negatively correlated with fitness in another. But in many organisms, the sexes do not become dimorphic until maturity – that is to say, juveniles all look pretty much alike, even when adults show clear differences between males and females. Which leads to the question: how does sexually antagonistic selection change over an organisms’ lifespan? Research from studies of Drosophila flies suggests that this is the case, but the question hasn’t been well-studied in vertebrates.

Everyone's favorite anole, Anolis sagrei

Everyone’s favorite anole, Anolis sagrei

Until now. In his Evolution talk, Aaron Reedy (University of Virginia) described his work testing whether sexually antagonistic selection changes over ontogeny using our favorite workhorse of evolutionary ecology, the brown anole (A. sagrei). Anolis sagrei are sexually dimorphic, with adult male body sizes up to 30% larger than females, but juveniles are monomorphic. Reedy and colleagues  sampled A. sagrei on several small islands in a Florida watershed four times a year, capturing thousands of adults and juveniles. They measured the body size of all lizards captured, and combined this morphological data with survivorship data to determine how selection was acting on body size in adults and juveniles.

They predicted that juvenile males and females would experience concordant selection, while adult males and females would experience antagonistic selection. And this is exactly what they found: for juveniles, body size was correlated with survival in the same way between sexes. But in adults, this was not the case. In the first year of sampling, there was no selection on body size for adult females, but positive selection for males, such that bigger males survived better. Interestingly, during the second year of sampling, the relationship flipped – females experienced positive selection on body size, and males experienced negative selection. The reasons for this shift are uncertain, but the main point is clear – sexually antagonistic selection does indeed change over ontogeny. Reedy et al. are planning to follow up this great new research by expanding their study to look at more islands and more traits to get at the finer points of these selective differences, so stay tuned!

Evolution 2017: It Doesn’t Pay to Be Risky When Predators Are About

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Oriol Lapiedra opened up the penultimate day of Evolution by discussing his results of a recent field experiment in the Bahamas. In this project, Lapiedra and colleagues evaluated how inter-individual variation in behavior – specifically risk-taking – influenced survival. To do this, the research team took advantage of a well-understood model system in evolutionary ecology: brown anoles (Anolis sagrei) on islands with and without anole-predators (curly-tailed lizards; Leiocephalus carinatus) in the Bahamas. Male and female brown anoles were collected and subjected to a behavioural trial which measured the amount of time it took for a lizard to leave a refuge after being exposed to a predator. These observations were used to quantify each individual’s propensity to take risks. For example, those individuals that left their refuge shortly after seeing a predator were interpreted as being more ‘risky’ than more conservative individuals. Following these trials, each lizard was x-rayed to assess morphology and individually tagged, before being released onto one of 4 predator-free islands or 4 predator-present islands, all of which were currently void of anoles.

Lapiedra et al. started with a priori hypotheses that overall survival would be lower on those islands with predators, and those that did survive would be individuals considered less risky. After waiting 4 months, the research team returned to the Bahamas to collect all lizards from each island and see which individuals had survived. The authors report that, as expected, overall survival was lower on islands with predators, and that there was a significant relationship between behaviour and survival such that high risk-taking individuals had much lower survival when predators were present. This suggests that under those biotic conditions, natural selection operates against those riskier phenotypes. On closer inspection, this relationship was largely driven by a strong relationship in females, with no significant relationship existing between risk-taking behavior and survival of males.

Lapiedra et al. then contrasted these results by independently assessing how morphology was related to survival. The authors found that both risk-taking behavior and morphology influenced survival, however – and, important to this study – the relative effect of an individual’s risk-taking behaviour was much more influential on survival.

Evolution 2017: Urban Lizards Are Larger but Show No Consistent Trend in Dewlap Area or Injury Rate

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At last night’s poster session, undergraduate Derek Briggs (U. Mass. Boston) presented findings from his senior capstone project in which he looked at several traits related to dominance and health. Using a dataset of x-rays and dewlap photos collected over a 4 year period from various urban and forest sites across Puerto Rico (by Kristin Winchell), Derek looked at body size, body condition, dewlap size, and injury rates (broken bones and missing digits) to see if there was a difference in frequency between urban and forest habitats.

Derek and his co-authors chose these traits because they thought they might be impacted by shifts in lizard density and distribution in the urban habitat which may lead to increased male-male competition. Specifically, in urban habitats, lizards tend to perch closer to one another because the potential perches are more clustered. This increase in local density could lead to increased encounter rates and fights over optimal perch sites, food resources, or mates. Derek hypothesized that this shift in distribution should lead to shifts in these traits, although he did not have a prediction about the direction of these shifts.

Derek Briggs with his poster.

Derek found that urban lizards were consistently larger than forest lizards in terms of snout-vent-length (SVL) but that body condition (mass~SVL) did not consistently differ between sites. Although all paired populations had significant differences in body condition, in some municipalities lizards were fatter in urban habitats and in some they were fatter in forests. In terms of dewlap size, Derek did not find any significant trends, although he still has quite a few dewlap photos to analyze still, so stay tuned!

In terms of injuries, Derek did not find significant differences between forest and urban animals for bone breaks or missing digits. However, these are rare events to begin with, so it is possible that a much larger sample size is needed to detect a difference. His findings do suggest a trend of more bone breaks in urban populations, and more missing digits in forest populations. He attributes this trend to either elevated male-male competition in urban habitats or differences in predator communities.

We look forward to seeing the full results from Derek’s honors thesis.

Evolution 2017: Urban Anoles Sprint Faster on Smooth Substrates

Kristin Winchell gives her talk on urban anoles at Evolution 2017.

Kristin Winchell gives her talk on urban anoles at Evolution 2017.

When I think of Puerto Rico, the first thoughts that come to mind are of sunny beaches and lush rainforests. There are, however, also lots of urban habitats in Puerto Rico. San Juan, for example, has two million human residents, and also lots and lots of anoles. Doctoral candidate Kristin Winchell has been studying adaptation in urban anoles for several years. Last year, she published1 her work showing that Anolis cristatellus in urban habitats have longer hindlimbs, bigger toe pads, and more lamellae than lizards in rural habitats.

A connection that was missing, however, was how the morphological shifts she documented related to performance differences in urban versus rural habitats. To get at this question, she conducted sprinting trials with different substrates to see how limb and toe characteristics affect sprinting capacity. Lizards in urban habitats use much smoother perches, such as fences and posts, and so the hypothesis was that the longer limbs and toe pad differences she detected improved sprinting performance on smoother substrates. She used three different substrates for sprinting trials – bark (rough surface), metal (smooth surface), and painted concrete (very smooth surface). She found that, overall, lizards sprinted more slowly on more slippery substrates. On average, lizards sprinted at 60% of their maximum capacity, indicating a strong performance hit when using slippery substrates.

Kristin confirmed that the urban anoles were better at sprinting on all substrates – including the slippery ones – than rural anoles. When she explored the results in greater detail, she found that only lamella number explained variation in sprint performance, with no appreciable effects of limb length or toe pad area. Kristin’s elegant study demonstrate how we can document evolution on recent timescales, and shows how urban environments provide strong selective pressures for the animals that live in them.

1. KM Winchell, RG Reynolds, SR Prado‐Irwin, AR Puente‐Rolón, LJ Revell. 2016. Phenotypic shifts in urban areas in the tropical lizard Anolis cristatellus. Evolution 70:1009-1022