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Article

Lizard Dewlap Color and Malaria Infection: Testing the Hamilton-Zuk Hypothesis

by
Tiffany M. Doan
*,†,‡,
Alexis D. Mingos
,
Aiden E. Juge
§ and
Melissa A. Simmons
Division of Natural Sciences, New College of Florida, 5800 Bay Shore Road, Sarasota, FL 34243, USA
*
Author to whom correspondence should be addressed.
†
Current address: Archbold Biological Station, 123 Main Drive, Venus, FL 33960, USA.
‡
Current address: Department of Biology, University of Central Florida, 4110 Libra Drive, Orlando, FL 32816, USA.
§
Current address: Department of Animal Science, Texas A & M University, College Station, TX 77843, USA.
Diversity 2023, 15(2), 209; https://doi.org/10.3390/d15020209
Submission received: 31 December 2022 / Revised: 30 January 2023 / Accepted: 31 January 2023 / Published: 2 February 2023
Browse Figure
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Abstract

:
The Hamilton-Zuk hypothesis indicates that parasites may have a negative effect on the appearance of sexual traits within an infected individual. Anolis sagrei, or brown anoles, are small invasive lizards common throughout Florida and many other areas where they have been introduced. The colorful dewlaps under the chins of males are used as a signal during territorial contests with other males and as an ornament to attract females. Anoles may be infected by the malaria parasite Plasmodium floridense. In this study, we investigated the relationship of malarial infection with dewlap color and spectral brightness of A. sagrei. We achieved this by capturing male brown anoles, taking blood samples to examine for malarial infection, and recording the color of their dewlaps. We found that the dewlaps of infected Anolis sagrei had duller coloration than the dewlaps of uninfected lizards. These results provide support for the Hamilton-Zuk hypothesis. Our results suggest that infection by P. floridense could potentially influence fitness of the lizards by reducing the expression of their color signals. Additional research on fitness effects of the malaria parasite on anoles is important for fully understanding this phenomenon.

1. Introduction

The Hamilton-Zuk hypothesis states that the visual quality of male sexual traits may be influenced by parasitic infection, resulting in potential fitness advantages for the males displaying traits that would indicate greater parasite resistance [1]. From this hypothesis, two predictions may be posed: The intraspecific prediction proposes that, within a species, males with higher showiness of traits have less parasitic infection; the interspecific prediction suggests that species with males displaying the most ornamental traits are species that have been subject to the highest rates of parasitism [1]. Although some studies have confirmed the hypothesis [2,3,4,5,6], others have found no relationship between parasitism and ornaments [7,8,9,10] or the opposite of the hypothesis’s prediction [11,12,13,14].
Hamilton and Zuk [1] proposed their hypothesis with bird coloration, but other studies have tested the hypothesis with coloration in fish [3,5,10], frogs [8], and reptiles [6,9,11,12,13,14]. In lizards, the intraspecific hypothesis was rejected with regard to Aruba whiptails (Cnemidophorus arubensis), which had more colorful bodies with greater haemogregarine parasitic infection than their uninfected counterparts [11]. Schall proposed that because the more colorful lizards in that species were also more active, they had greater opportunities to be exposed to the arthropod vectors [11]. Male Algerian psammodromus lizards (Psammodromus algirus) had greater red surface area on the face in the non-parasitized population than the tick-parasitized population, but the opposite trend was true for red color saturation on their heads [6]. After experimentally injecting Psammodromus with bacterial material, the non-parasitized population had a decrease in red surface area and the tick-infected lizards had a decrease in red color saturation [6]. Psammodromus male individuals from the parasitized population that displayed sexual ornamentation were larger, had fewer parasites, and had greater color saturation than others in their population [6], demonstrating that coloration was an honest signal in that species and supporting the Hamilton-Zuk hypothesis. Schall and Staats tested body and dewlap color of anole lizards infected with blood and intestinal parasites across species from islands in the Caribbean Sea and found no support for the interspecific prediction of the Hamilton-Zuk hypothesis [9]. Thus, the Hamilton-Zuk hypothesis has received mixed support in tests with lizards [14].
Anoles are small New World lizards that possess a dewlap, a sexually dimorphic flap of skin located beneath the chin, that may be extended and retracted to communicate with potential competitors, predators, or mates [15,16]. Anole dewlaps likely function both for territorial signaling and courtship behavior, making dewlaps both armaments and ornaments, which has been supported by multiple studies (e.g., [16,17,18,19]). But some researchers have found no association between dewlap extension and courtship [20,21]. Dewlap extension has been shown to be an honest signal with respect to body size and body condition [22,23].
The role of dewlap color as an important aspect of territorial signaling was also demonstrated in that the winner of male-male interactions of brown anoles displayed more frequently and had dewlaps that had the most ultraviolet reflectance, orange, and red colors [24]. Female preference for red dewlaps has been demonstrated experimentally [19]. Dewlap color in anoles is caused by pteridine and carotenoid pigments, which combine to produce colors in lizards [25,26]. Although pteridines may be synthesized by the animals, carotenoids must be obtained from the diet [26,27], which A. sagrei acquire from eating phytophagous insects [25]. Carotenoid pigment deposition in lizards has been hypothesized to be a marker of environmental quality [27,28]. Unlike some lizards [27], it does not appear that anoles can substitute pteridine pigments in their dewlaps if carotenoids are lacking [29]. Some aspects of dewlap color have also been found to predict aspects of anoles’ health, including body condition, immune response, and hematocrit in males [30].
Brown anoles, Anolis sagrei, which are native to several Caribbean islands, are an invasive species throughout the southeastern United States and other parts of the world [31]. Male brown anoles have dewlaps that appear mostly red in color but have areas of yellow and orange patterning in the central area with white and ultraviolet around the margin [24,30,32,33,34]. Diversity of dewlap patterns is influenced by a combination of natural selection, sexual selection, and interspecific recognition [32], with dewlap color and pattern varying because of the presence of predators and climatic moisture gradients [32,33].
The malaria parasite Plasmodium floridense has been found to infect brown anoles in Florida, USA, and other areas [35,36,37,38]. A study of P. floridense prevalence indicated that it is most common in brown anoles along the coast of the Gulf of Mexico, near urban areas, and in places where fresh water is available [35]. Infection prevalence was found to vary seasonally [36,37]. Doan et al. found that Anolis carolinensis had higher infection prevalence than A. sagrei in Central and Southwest Florida [37]. Bessa et al. determined that infected brown anoles had an elevated immune response in relation to uninfected lizards, at least in Central Florida [38].
Few studies have tested the Hamilton-Zuk hypothesis with malarial parasite infection, and the Hamilton-Zuk hypothesis has not been tested on anole dewlaps [14]. Fence lizards infected with Plasmodium mexicanum exhibited more black pigmentation on their ventral surfaces than in uninfected lizards [39]. However, the differences were subtle and would only marginally improve a female’s chance of choosing a non-infected lizard as a mate [39]. In the current study, we conducted a test of the Hamilton-Zuk hypothesis by investigating the relationship between dewlap color in A. sagrei and malarial infection by P. floridense in Florida. Because in A. sagrei dewlaps are only possessed by males and are colorful, brown anole dewlaps are secondary sexual characteristics ripe for testing the hypothesis. Anolis lizards are thought to have color vision akin to that of humans, in addition to the ability to see ultraviolet light [40]. Thus, it can be inferred that spectral brightness and color of dewlaps will be similarly perceived by both humans and A. sagrei. We expected that infected lizards would be less colorful (less red and more white) than uninfected lizards in accordance with the Hamilton-Zuk hypothesis. We predicted this because parasitized lizards may have secondary sexual characteristics of reduced attractiveness and dewlap color may serve as an honest indicator of individual health and condition. Therefore, more resources may be allocated to combating infection and less may be used to provide pigment for showier coloration [22]. Investigating the effects of Plasmodium infection on A. sagrei is important for testing the classic hypothesis and for understanding the biology of an invasive species now ubiquitous in Florida.

2. Materials and Methods

2.1. Field Methods

We captured male Anolis sagrei Duméril and Bibron, 1873, in Duval, Seminole, and Sarasota counties, Florida, USA, by hand. Males were adults and subadults with extensible dewlaps. After capture, OrajelTM (Church & Dwight, Inc., Ewing, NJ, USA) was applied to the third toe of the hind foot as an anesthetic [38]. While waiting for the toe to become numb, we measured the snout–vent length (SVL) with electronic calipers in mm and then used a Color Muse color matching handheld colorimeter and color matching mobile application (Variable Inc., 2019; Chattanooga, TN, USA) to quantify RGB (red, green, blue) color values from the dewlaps of the live captured anoles. The lizard dewlaps were extended using tweezers or by hand, and three measurements of RGB intensity values were taken from each lizard (two on one side of the dewlap and one on the other side) in the approximate center of the dewlap by holding the colorimeter at a 90° angle approximately 3 mm away from the dewlap. To determine Plasmodium infection status, we obtained blood samples from each anole by clipping the toe with scissors [37,38]. Lizards were processed in less than 5 min each. Plasmodium floridense is the only saurian malaria species that occurs in Florida [35] and we identified the parasites using Telford as a reference [41]. After data were collected, all lizards were euthanized with isoflurane in accordance with Florida Fish and Wildlife Conservation Commission nonnative species guidelines. The blood samples were fixed and stained using the Hema 3 Stat Fix Kit. Under 1000X magnification, we examined slides for parasite presence for 5 min each to determine infection status [36]. The project was completed under IACUC protocol IS00008673.

2.2. Analysis Methods

Color may be broken down into two major components, chroma and luma [42]. Chroma of a particular color [43], is the intensity or saturation of a particular wavelength (color), whereas luma is the spectral brightness of an image, perceived as white [42] because no color is absorbed. We were interested in parasite-related differences in both the red chroma values (red color saturation) and in overall spectral brightness. We tested the brightness of RGB color intensity values by quantifying them through the formula ([Y] = 0.2126 R + 0.7152 G + 0.0722 B) for relative brightness, or luma, which represents the brightness in an image irrespective of color [43]. Luma was found for each RGB color trial, and averaged per lizard, using the formula for relative brightness.
To determine if infection is a predictor of dewlap color (luma and/or red saturation) in Florida Anolis sagrei, we used a generalized linear model utilizing a gamma distribution with a log link function in IBM SPSS Statistics version 28. We ran two separate tests of dependent variables, one for luma and one for red chroma. For each, we tested three a priori candidate models. We included lizard SVL as a covariate because some studies have shown that lizard body size may be related to infection status [37,44,45]. We included models that had the factors plus interactions between SVL and infection status (Table 1). We evaluated the models with AICc scores and ranked alternative models with AICc weights, considering models to have support when ΔAICc < 2 units from the highest ranked model [46]. Means are presented ± SD.

3. Results

We tested 97 male A. sagrei (82 uninfected and 15 infected). Male lizards ranged from 32.5 to 76.7 mm SVL (mean = 53.01 ± 8.9 mm). Average luma was significantly lower (i.e., brighter) for infected lizards (120.13 ± 21.9) than uninfected lizards (132.31 ± 31.0) (Figure 1). The candidate model for luma with the highest AICc weight was infection with SVL (Table 1). No other models had support (i.e., all other models had ΔAICc > 2.0).
Red color values differed slightly but not significantly between infected and uninfected lizards (infected mean = 137.38 ± 22.4; uninfected mean = 150.76 ± 34.6), with redder dewlaps belonging to uninfected lizards. The model for red color with the highest support was infection and SVL, but the infection only model also received support (Table 1).
There was a large amount of variation of dewlap color (both luma and red chroma) within uninfected lizards (Figure 1), encompassing the entire range found in the infected lizards. In fact, the two lowest luma scores were from uninfected lizards. Those two lizards had yellowish dewlaps with little obvious red coloring. Even with the high variance of the uninfected lizards, we still found differences in mean luma and mean red chroma.

4. Discussion

4.1. Test of the Hamilton-Zuk Hypothesis

Our research provided support for the intraspecific prediction of the Hamilton-Zuk hypothesis [1]. Dewlap red color values trended lower for A. sagrei infected with P. floridense, in agreement with the hypothesis. Moreover, average luma was significantly lower (higher spectral brightness) in infected lizards, which also matches the prediction of the Hamilton-Zuk hypothesis (but see below). Coloration of secondary sexual characteristics may have been diminished by parasitism, as was shown by Milinski and Bakker, but most studies have found no effect (e.g., [22]) [5]. Cook et al. similarly found that brighter anoles of a related species had higher ectoparasite loads than duller lizards [22]. In both our study and Cook et al., male anoles who were infected with parasites tended to have brighter dewlaps than their uninfected counterparts [22].

4.2. Methodological Differences from Previous Studies

As pointed out by Megía-Palma et al., many previous authors used the term “brightness” in a way that clouded their interpretation of their conclusions in light of the Hamilton-Zuk hypothesis [14]. Some authors used the term brightness when examining photographs of animal coloration [2,9,12] as the perceived intensity of a color as received from a visual stimulus [42]. However, perceived brightness is affected by multiple factors, including individual physiological variation in human observer photoreceptors, background color, and lighting [42]. Hamilton and Zuk and Read equated the term “showiness” with brightness, when in fact showiness is probably the opposite of actual spectral brightness because brightness means whiteness and something colorful has low brightness [1,2,43]. Many authors followed in equating showiness or colorfulness to brightness (e.g., [5,12,47]), which has obfuscated the patterns that have been found. Once researchers began to use colorimeters or spectrophotometers to measure color saturation and/or spectral brightness, they often claimed patterns that contradicted the Hamilton-Zuk hypothesis, sometimes because of differences in terminology or method of assessing “brightness”. For example, Molnár et al. measured the brightness of throat colors of Lacerta viridis with a spectrometer and found lower spectral brightness (and therefore higher color saturation) in infected lizards but misinterpreted their results to support the Hamilton-Zuk hypothesis [13] (see [14]). We contend that analyzing both luma and chroma [43] via a colorimeter or spectrophotometer allowed for a more complete picture of both brightness and color as it is perceived by humans and lizards.

4.3. Mechanisms of Color Differences

Because infected lizards have brighter dewlaps than uninfected lizards, the mechanisms behind this phenomenon present a chicken-and-egg problem [48]. Does Plasmodium infection cause a change in a lizard’s dewlap color, or are lizards with particular dewlap colors more likely to be infected with Plasmodium? The immunocompetence handicap hypothesis posits that there is competition for resources between the immune system and secondary sexual characteristics [49,50], which is supported by various studies. For example, experimental infection of guppies caused a decrease in red coloration, which led females to decline to select them for mating [5]. In lizards, after experimentally challenging male Psammodromus algirus by injecting them with bacterial lipopolysaccharide, the surface area of red coloration on the lizards’ heads changed [6]. However, the majority of tests of the Hamilton-Zuk hypothesis are simply correlational without examining the proximate causes of the differences (but see [45]). Parasites may directly use host resources, altering a lizard’s coloration [22]. These effects may be mediated by testosterone or other hormones [49]. Testosterone, which is responsible for the development of secondary sexual characteristics such as dewlap size and color [51,52,53], can decrease or impair the immune system’s response to parasitic infection [49,54].
Alternatively, immune responses to the parasites may alter coloration. McGraw and Ardia found that novel antigens caused a reduction in the circulation of carotenoid pigments in birds, reducing their ability to allocate the pigments to tissues because the pigments are used in mounting immune responses [55]. This sets up a tradeoff between pigment deposition for ornamental coloration and immune function so that coloration may be an honest signal of an individual’s level of parasite infection [6,22,48,55], in support of the immunocompetence handicap hypothesis and the Hamilton-Zuk hypothesis. On the other hand, Steffen et al. found that dewlap carotenoid pigmentation did not change in A. sagrei during nutritional stress or food supplementation with carotenoids, which suggests that dewlap color may not be as labile as carotenoid pigmentation in other animals such as guppies and zebra finches [55,56,57]. Dietary carotenoids have been shown to be immunostimulatory in some species [55].
Another possibility for the differences in spectral brightness between infected and uninfected lizards could be that the vectors carrying P. floridense detect a difference in bright lizards (or less red lizards, or both) and bite them more often. It is known that mosquitos can sense qualities of their potential hosts and select certain individuals over others [58,59,60]. If the vectors are sensing a trait linked to dewlap coloration, they may select particular lizards to feed upon (and infect with Plasmodium), which produces a bias in infection incidence connected to dewlap color. Mosquitos innately prefer to rest on dark surfaces [60], which could attract them to darker dewlaps that have more color saturation than brighter dewlaps. However, this is directly in opposition to the results of our study in which lizards with brighter dewlaps were more likely to be infected with Plasmodium. A recent study on color preference in Culex mosquitos (the genus assumed to contain the vector of P. floridense; [61,62]) found that they were attracted to black, blue, and green, but not red or any of the other colors tested [63]. Another study that examined C. nigripalpus found that out of the colors tested (which did not include black) mosquitos fed longest on green artificial hosts, with white being fourth place and red being fifth [59]. Based on those data, it does not appear that mosquito vectors are selecting host lizards based on coloration, but we cannot discard the possibility that they may be selecting lizards with a trait linked to coloration such as aromas of carotenoids [64].
One trait that appears to be linked to dewlap coloration is size of the lizards as we found that SVL was one of the factors in our top models for both luma and red chroma. As discussed by Bessa et al., larger lizards may be more likely to be bitten by mosquitoes because they have a larger surface area for bites and may be more active [38,44,58]. As Plasmodium infection in Anolis sagrei may be chronic, older and larger lizards may be more likely to be infected [36,38]. Without experiments introducing infection into lizards or selection experiments with insect vectors, there is no way to determine if Plasmodium is the physiological cause of the difference in color between infected and uninfected lizards or if the difference is caused by vector selection. Further study is required into whether P. floridense caused a greater perceived brightness of dewlap color in the brown anoles of our study.

5. Effects on Fitness

In most cases where the Hamilton-Zuk hypothesis has been supported, the parasite has a known negative effect on fitness [4,5], but it has not yet been definitively determined whether P. floridense has significant negative effects on the fitness of A. sagrei [37,38]. However, as there was a difference in dewlap brightness in brown anoles infected with P. floridense and uninfected individuals, this may be additional evidence that the parasite does have significant effects on lizard health and/or fitness.
The dewlap color of male brown anoles has been shown to be directly related to health condition [33] and the ability to win behavioral contests [24]. Additionally, Anolis carolinensis females prefer males with red dewlaps over experimentally altered colors [19], and other studies have shown that lizards can discriminate continuous variation in orange/red coloration [65]. Many animals have reduced display rates (e.g., [66]) and reduced aggression when parasitized (e.g., [67]). Anolis brevirostris that were more heavily parasitized displayed less frequently than lizards with fewer ectoparasites [22]. Based on our project demonstrating that male brown anoles have brighter dewlaps, parasitized males may have reduced ability to defend territories or to attract mates, in support of the intraspecific prediction of the Hamilton-Zuk hypothesis [1]. Previous research has shown that parasitism of P. floridense on A. sagrei was related to differences in leukocyte profiles, potentially decreasing the health of infected lizards [38]. If this parasitism reduces health, decreases males’ success in territoriality, and decreases attractiveness to females, Plasmodium infection has the potential to greatly lower the fitness of parasitized brown anoles.
Further research examining the fitness effects of P. floridense on A. sagrei is necessary, to examine both the ultimate and proximate mechanisms of the relationships between spectral brightness and red coloration of anole dewlaps and parasitism. Examining reproductive success after experimental infection would answer many of the questions inspired by this project, but this is currently not possible because the vector of P. floridense in Florida remains unconfirmed [37,61,62]. Additional research on the longevity of Plasmodium infection in anoles, the vector, and changes in coloration over time in individuals would give us further insight into the mechanisms behind increased spectral brightness and decreased red coloration associated with Plasmodium parasitism in brown anoles, a key invasive species in many locations around the world.

Author Contributions

Conceptualization, T.M.D.; methodology, T.M.D. and A.D.M.; validation, T.M.D.; formal analysis, T.M.D. and A.D.M.; investigation, T.M.D., A.D.M., A.E.J. and M.A.S.; resources, T.M.D.; data curation, T.M.D.; writing—original draft preparation, T.M.D., A.D.M., A.E.J. and M.A.S.; writing—review and editing, T.M.D.; visualization, T.M.D.; supervision, T.M.D.; project administration, T.M.D.; funding acquisition, T.M.D. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by New College of Florida 2020.

Institutional Review Board Statement

The study was approved by the Institutional Review Board of the University of South Florida IACUC (IS00008673).

Data Availability Statement

Raw data may be obtained from the corresponding author upon request.

Acknowledgments

We would like to thank Carson Broadwater, Dria Anderson-Whittaker, Lexi Fox, Moriah Olsen, Natalie Kornblum, Oceanna Krasny, and Joshua R. King for help catching lizards and providing additional laboratory data to us. We also thank lizard dogs Matilda and Monte for cornering lizards and assisting with their capture. We thank the students in the Foundations of Biology Laboratory courses for assisting us with lizard capture and field data collection.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Box-and-whisker plot of (A) average luma values and (B) average red chroma values for Anolis sagrei infected and uninfected with Plasmodium floridense in Florida, USA. The inner boxes represent the second and third quartiles, whereas the whiskers represent the first (upper) quartile and the fourth (lower) quartile. The lines within the boxes are the medians and the Xs represent the means. Dots display outliers for uninfected lizards. Average luma was significantly different between infected and uninfected lizards whereas average red chroma was not significantly different.
Figure 1. Box-and-whisker plot of (A) average luma values and (B) average red chroma values for Anolis sagrei infected and uninfected with Plasmodium floridense in Florida, USA. The inner boxes represent the second and third quartiles, whereas the whiskers represent the first (upper) quartile and the fourth (lower) quartile. The lines within the boxes are the medians and the Xs represent the means. Dots display outliers for uninfected lizards. Average luma was significantly different between infected and uninfected lizards whereas average red chroma was not significantly different.
Diversity 15 00209 g001
Table
Table 1. Results of models considered with luma and chroma as the dependent variables in two separate tests. The models explain the likelihood of dewlap color in Anolis sagrei individuals in Florida, USA, with regard to infection by Plasmodium floridense and body length (SVL).
Table 1. Results of models considered with luma and chroma as the dependent variables in two separate tests. The models explain the likelihood of dewlap color in Anolis sagrei individuals in Florida, USA, with regard to infection by Plasmodium floridense and body length (SVL).
ParametersdfLog LikelihoodAICcDelta AICcAICc WeightOmnibus Chi SquareOmnibus Chi Square p
Luma: Infection, SVL2−454.944918.32200.651877.9150.019
Luma: Infection, SVL, Infection X SVL3−454.943920.5462.2240.214407.9150.048
Luma: Infection1−457.616921.493.1680.133732.570.109
Red: Infection, SVL2−467.578943.59200.446504.9790.083
Red: Infection1−468.836943.9310.3390.376892.4630.117
Red: Infection, SVL, Infection X SVL3−467.394945.4471.8550.176615.3490.148
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Doan, T.M.; Mingos, A.D.; Juge, A.E.; Simmons, M.A. Lizard Dewlap Color and Malaria Infection: Testing the Hamilton-Zuk Hypothesis. Diversity 2023, 15, 209. https://doi.org/10.3390/d15020209

AMA Style

Doan TM, Mingos AD, Juge AE, Simmons MA. Lizard Dewlap Color and Malaria Infection: Testing the Hamilton-Zuk Hypothesis. Diversity. 2023; 15(2):209. https://doi.org/10.3390/d15020209

Chicago/Turabian Style

Doan, Tiffany M., Alexis D. Mingos, Aiden E. Juge, and Melissa A. Simmons. 2023. "Lizard Dewlap Color and Malaria Infection: Testing the Hamilton-Zuk Hypothesis" Diversity 15, no. 2: 209. https://doi.org/10.3390/d15020209

APA Style

Doan, T. M., Mingos, A. D., Juge, A. E., & Simmons, M. A. (2023). Lizard Dewlap Color and Malaria Infection: Testing the Hamilton-Zuk Hypothesis. Diversity, 15(2), 209. https://doi.org/10.3390/d15020209

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