Category: New Research Page 21 of 67

Female Anolis sagrei

In recent months, there has been a lot of talk on the Auburn campus about multimodal signals. Diana Hews gave a phenomenal seminar to the Biology Department last November about complex signaling in Sceloporus lizards, and just last week Eileen Hebets told a similar story about signaling behavior in a group of invertebrates, amblypygids. The latter lecture prompted a momentary side conversation between a Warner Lab postdoc, Tim Mitchell, and me concerning the apparent lack of multimodality in Anolis signaling. Ironically, I just ran across a 2016 publication by Baeckens et al that forced me to eat crow, albeit only a tiny bit of crow.

Anoles, like most iguanians, have been labeled as “visual only” signalers and for good reason. Anoles lack the epidermal glands that secrete the typical chemicals used in lizard chemosensing. Rather, anoles are known widely as models for communication for their reliance on visual signals (which have been demonstrated to be quite complex despite being unimodal) and are also characterized by a low baseline rate of tongue-flicking, even when considered against the backdrop of other visually oriented iguanians. Additionally, previous experiments conducted with A. carolinensis found no significant evidence of chemosensory function in prey selection, assessment of opponents, or in mate choice (Jaslow & Pallera, 1990; Forster et al., 2005; Orrel & Jenssen, 2002). The question of whether or not anoles utilize chemical signals seems to be one answered; however, Baeckens et al have conducted a simple but convincing study that might demonstrate the converse.

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In trying to understand the evolution of visual signal diversity we are often faced with problem of asking which of two possible signals is most visible against a particular natural background. Alternatively we may want to know how easily different signals (for example signals of sympatric species) can be told apart.

When animals use colorful signals to communicate with conspecifics, selection will tend to favor colors that are highly visible against the natural background and colors that can easily and unambiguously be distinguished from signals utilized by other similar-looking species. Thus, in order to understand the evolutionary pressures on signal properties, we often want to know how distinct two different colors appear to an animal viewer. Perception of color by most animals differs from human perception because of differences in visual-system anatomy and physiology. How, then, can we quantify the difference in appearance of colors to an animal viewer?

A useful approach is to quantify the perceived difference between color stimuli as a distance in the animal’s “perceptual color space.” This refers to some measure of the difference in sensory stimulation elicited by different colors. At present most studies of visual ecology and communication use one of two methods to measure perceptual color space distance between pairs of colors. The first involves determining the relative stimulation of the different classes of cone photoreceptors by each color stimulus in units of relative photon capture, plotting colors in n-dimensional space (where n is the number of photoreceptor classes), and then measuring a simple Euclidian distance between the points. The second approach involves estimating the noise within each photoreceptor channel, determining the detection threshold – defined as the just-noticeable difference, or JND, between the two colors – determined by photoreceptor noise, and then estimating the distance between two colors in units of multiples of this threshold, or in units of JNDs. The photoreceptor noise method has been shown to be effective for estimating color discrimination thresholds, but the idea that differences between supra-threshold colors can be measured in multiples of the JND is more controversial. Each of these methods has some theoretical support, and each has advantages and disadvantages in terms of assumptions required and the information needed to do the calculations. However, empirical tests of which method works best are lacking, and there is not much agreement on the best way to measure perceived differences between colors that are well beyond the threshold for discrimination.

What we need here is a model system – and that usually means anoles! Anoles have an excellent, well-understood color vision system. Moreover a method has been developed that uses visual attention as an assay of signal visibility. Fleishman et al. (2016) used this method to quantify the visibility of different colors viewed against a gray background by Anolis sagrei. They then used these behavioral results to test the accuracy of the two different popular methods of measuring distance in visual color space. In these experiments anoles viewed a checkerboard of gray squares in their visual periphery (Fig. 1). One square was then abruptly shifted to some other color. The distance in color space from the initial gray to the newly appearing color was determined using the two different metrics described above. The probability of a gaze shift towards the novel colored stimulus was quantified, and colors throughout the anoline color space were tested. The probability of detection was then plotted against the different measures of perceptual color distance.

Figure 1. (a) Lizard sits on the perch in a small cage. The experiment waits until its gaze is directed straight outward towards the video camera (t1). At t2 a small colored stimulus square is presented in the middle of the checkerboard visual field. The camera records whether or not the lizard notices the newly introduced color-square and shifts its gaze towards it. See the video above. The video at the top of the page illustrates the appearance of the stimulus to a lizard and shows a positive response.

Which method best predicted the results? It turns out both methods gave excellent predictions of the behavioral data! In this case anoles are the peacemakers. Basically, the information available to the color vision system is how much difference there is in the photon capture by different cone classes exposed to different colors. These two different ways of quantifying this change turn out to give rather similar predictions, and both sets of predictions accurately predict detection probability. Thus the anoles give a firm go ahead for both methods of modeling distance in color space. The ability to easily model distances between colors in anoline perceptual color space should greatly facilitate studies of the evolution of dewlap color diversity because we can easily figure out which color is most visible under each set of natural habitat light conditions.

Now we just have to figure out why Anolis dewlaps come in so many different colors!

Anolis gundlachi from The Reptile Database

Plasticity is the ability of one genotype to produce multiple phenotypes under different environmental conditions. Once considered a hindrance to the study of evolution, plasticity is now thought to be one basic way organisms may persist in novel habitats long enough for adaptation to occur. Because of its propensity for rapid change, behavioral plasticity is considered one of the most effective ways that organisms can adjust to new surroundings. In some circumstances, behavioral changes can even be immediate. In example, some populations of birds can alter their vocalizations when singing against the backdrop of city noise pollution (Potvin and Mulder, 2013). This ability to instantaneously respond to external stimuli is known as contextual plasticity, and it may be a powerful tool by which organisms adapt to novel conditions. 

A new paper by Ord et. al., explores the potential use of contextual plasticity in social communication using species of Puerto Rican Anoles. Anoles use visual signals (head bobbing, pushups, and dewlapping) to communicate with one another, and previous research has noted that these signals are in competition with background visual noise (i.e. presence/movement of leaves and visual obstructions) and their reception is more challenging under low light conditions (Ord et.al., 2007). Anoles must adjust their signaling behavior in order to compete with distractions in their environment. The point of visual signaling is to be seen, so a positive relationship exists between mean visual noise and signaling speed and a negative relationship between mean display duration and mean light levels. See the decibel chart  which is used  to measure the intensity of a sound.

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Liolaemus lemniscatus. Photo from Thomas Kramer’s flickr account.

Based on thermal constraints, as deduced from the effects of global warming on key aspects of thermal biology (e.g. field and laboratory temperatures, and thermoregulation indices; after Hertz et al., 1993), Dr. Piantoni and Dr. Navas from the University of São Paulo, Brazil, and Dr. Ibargüengoytía from the University of Comahue, Argentina, assessed the vulnerability of a sample of populations from the genera Anolis, Liolaemus, Sceloporus, and Tropidurus  from a broad range of ecological settings such as the deserts of Yucatan, the Brazilian Cerrado, the lowlands of southern Patagonia steppe, the rainforests of Puerto Rico and the Nothofagus forests in Tierra del Fuego. The combined data on the four iguanian lineages, reported in a just-published paper in Animal Conservation, corroborate the hypotheses of increased susceptibility to warming in species from lower latitude and lowlands, and contributes to debate climate-related risk of extinction in lizards.

Thermoregulatory behavior increases with latitude and altitude and tropical and lowland environments are mainly occupied by thermoconforming lizards. In most of the cold and temperate environments (e.g. inhabited by Liolaemus and Anolis), warming could be neutral or beneficial and vulnerability to climate warming is not only linked to the efficiency of thermoregulation, but also to the high geographic and seasonal variation in the thermal biology of these species. Near the equator, susceptibility to climate change is associated with the tendency to physiological specialization as a result of the thermal stability of the forested environment and of the high proportions of operative temperatures exceeding the critical thermal maximum of most lizards of the open environments. The substrate temperatures at these localities will further increase with warming and eventually achieve overheating values. Whereas thermal shelters may assist lizards in the short-term, the compromise between sheltering and activity time may affect fitness in the long-term.

Overheating become a concrete risk in these environments, both as a direct driver of death or as a limiting factor for activity. Although a recent study on A. sagrei confirmed that some tropical populations might be capable of adapting to warmer and thermally variable environments (Logan et al., 2014), adaptive trends are unlikely to outrun global warming. Besides, habitat fragmentation and transformation may constrain the possibilities to disperse to cooler environments accelerating the extinctions, particularly in montane populations that would also face the upward progress of lowland species.

Adult specimen of Tropidurus torquatus from Tocantins, Brazil

Finally, it should be noted that the studied populations are potentially challenged by additional disturbances. Tropical populations, especially the ones inhabiting open and low elevation sites, are also vulnerable to the increasing fragmentation of the landscapes. For example, in Puerto Rico, species like A. cooki, which used to inhabit the dry forests, have been slowly displaced to areas in sympatry with A. cristatellus (Genet, 2002). The Brazilian savanna is gradually being replaced by soy fields and cattle ranches which may raise the soil temperature well above the predicted values and confine populations, such as Tropidurus torquatus‘ in Tocantins, to gallery forests. Paradoxically, the species with the highest vulnerability seem to inhabit the least protected areas, which emphasizes the urgent need of mitigation measures as the increase in conservation units to protect their underestimated biodiversity.

Ariel Kahrl, Christian Cox, and Bob Cox.

Sperm morphology is highly variable across animals and is a great model for studying the evolution of sexually selected traits.

Ariel Kahrl, a Ph.D. student in Bob Cox’s lab at the University of Virginia, gave a talk on a study which she and coauthor Cox did just that. They sampled sperm from native and introduced populations of Anolis sagrei, A. distichus, and A. cristatellus to look at variation in morphology.

Variation in sperm morphology between native and introduced populations of three Anolis species.

Interestingly, they found that introduced and native populations often varied in sperm morphology (i.e., head, midpiece, and tail lengths). Moreover, these effects were consistent between the three species tested!

Kahrl also pointed out that the variation observed in sperm morphology between males of a single species was often as large as that observed between different species. This study suggests that sperm morphology is highly plastic and/or is capable of rapid evolution in response to environmental change. Further work is needed to elucidate what selective pressures are driving the variation observed between introduced and native populations of these three species.

Brittney Ivanov at SICB 2016

Color changing behavior has been widely documented in many lizard taxa.For example, the green anole (Anolis carolinensis) can rapidly transition from a uniform green to brown-colored. In those taxa where color change is rapid (including the green anole), such behavior has been attributed to communication of socially relevant information such as aggression or dominance.  However, what information is conveyed through color change in A. carolinensis during social interactions remains an open question. Brittney Ivanov, a research technician in Michele Johnson’s lab at Trinity University performed experiments in captivity using lizards captured from the wild to examine this question.

Brittney captured 12 lizards of each sex, which were checked daily for coloration to assess the predominant coloration of each individual. She then paired lizards from the opposite sex and placed them together for 2 weeks to determine if coloration is used differently between naïve and novel pairs. Lastly, same-sex trials were performed in both male and female lizards to determine if coloration indicates higher social status.

Brittney found that males spent more time being green compared to females and that their predominant body color was consistent across social context or housing condition (living alone versus with a female). Predominantly green males also “won” more often in same-sex trials. Female coloration was not associated with the results of the same-sex trials, but females were found to be green more often when housed alone than when housed with a male. Brittney’s research suggests that coloration may be used differently between male and female green anoles and that for males, coloration may determine social status or competitive ability.

Austin Garner, an undergraduate at the University of Akron.

Anoles, geckos, and some species of skinks have adhesive toepads that allow them to cling to substrates. This adhesive ability is remarkable – anoles, for example, can hang from a glass pane using just one toe. Gecko adhesion is particularly well studied, but most research has focused on how these animals cling to dry surfaces. In their natural habitats, however, geckos often have to contend with wet surfaces.

Austin Garner, an undergraduate at the University of Akron working with Peter Niewiarowski, wanted to know whether geckos could move effectively on wet substrates. He measured sprinting performance in two species of gecko, Gekko gecko and Chondrodactylus bibronii, across a 2-meter vertical racetrack that was misted with water. Average sprint velocity on wet substrates did not differ significantly from the average sprint velocity on dry substrates, indicating that geckos can sprint equally fast on slippery surfaces. The substrate material, however, influenced how often geckos slipped. Geckos slipped more on glass substrates compared to acrylic substrates. Austin hypothesized that this is likely due to the surface chemistry of glass. Glass is a hydrophilic substrate, meaning that water is attracted to its surface more so than the surface of acrylic. Interestingly, the frequency of slipping differed among species. Chondrodactylus bibronii, a species of gecko from an arid habitat, slipped more often than G. gecko, a gecko found in the tropics. Although C. bibronii slipped more on wet substrates, this species did not suffer a decrease in average sprint velocity on wet substrates. This suggests that C. bibronii is somehow compensating for the slipping observed on wet substrates, but Austin is unsure of the mechanism behind this compensation. Overall, his study suggests that geckos can travel on wet substrates up to 2-meter without a reduction in their adhesive ability, and that at least one species of gecko can compensate for any loss of traction caused by the presence of water.