Natural parasites, rival’s color, and rival’s behavior explain aggression in a lizard

Male competition conforms to a cost-benefit model because aggression may increase reproductive prospects while increasing risks of injuries. We hypothesize that these agonistic interactions can also incur in energetic trade-offs in parasitized hosts. We staged dyadic male contests in the lab to investigate the relationships of multiple parasites with the agonistic behavior of lizard hosts, Sceloporus occidentalis. We also included in the analyses both color and behavioral traits from rivals because (i) color patches of lizards may serve as intraspecific signals used by conspecifics to assess the quality of opponents, and (ii) contests between male lizards fit classical models of escalated aggression, where focal lizards increase aggression displays in response to a rival’s behavior. Based on multimodel inference applied to mixed models, lizards displayed more pushups when they had more ticks and also when rivals performed more lateral compressions. The higher aggression in infested lizards might be explained as a correlate of host reproductive effort. Moreover, lizards infected by hematic coccidians performed fewer pushups, conforming to our initial hypothesis. Interestingly, focal lizards also displayed fewer pushups when the chroma and size of rival’s blue patch were greater. The results support the role of the blue patch of S. occidentalis as a sexual armament, because it contributes to the deterrence of aggression from rivals. They also revealed that natural infections in lizard hosts can contribute to explain their agonistic behavior. We encourage to account for natural infections in behavioral tests with lizards

April and June, 2014. UCSC. Thermal preferences and parasites of Sceloporus occidentalis bocourtii.

We captured 77 adult (males = 47, females = 30) coast range fence lizards, Sceloporus occidentalis bocourtii (Squamata: Phrynosomatidae), at Santa Cruz County, CA, USA (36.9852, -122.0614) during two sampling campaigns in 2014. In mid April we captured 42 lizards and in early June 35 lizards. All lizards were caught using a noose and were transported to the lab facilities in a cooler. The sex of the individuals was determined by the presence of enlarged post-anal scales (Cox et al., 2005; Megía-Palma et al., 2018). Snout to vent length (SVL) of the lizards was measured with a ruler to the nearest millimeter and their mass to the nearest gram using a digital scale. A body condition index was estimated using the Scaled Mass index (SMi). This estimation accounts for the growth effect on body size as well as for the scaling relationship between mass and body length (Peig and Green, 2009; 2010), and it is calculated using the standardized major-axis of the mass on body length (following Bohonak, 2004). A second mass measurement of the lizards captured in April (N = 42) was taken 11 days post-capture. Thus, during this period, the lizards were housed individually in plastic terraria with a damp substrate of peat moss and sand, and were provided with water and food (crickets dusted with vitamins and calcium) ad libitum. The terraria were kept in an environmental chamber with a 12L:12D photoperiod provided by natural spectrum fluorescent and ultraviolet lights and a cycling thermal regime. We used one empty terrarium with substrate to register standard temperatures 24 h/day every 5 minutes during 11 days with a data logger (hobo U23-002, Onset, Cape Cod, Massachusetts, USA). We set one probe of the data logger in one corner of the cage under the heat source (i.e., 40 Watt bulb) and other probe in the opposite corner.Within two days of capture lizards were allowed to select temperatures in experimental thermal gradients (i.e., 48-25 ºC) and their body temperature was recorded every minute during the 120 minute trial (as in Paranjpe et al., 2013). Preferred temperature (Tp) was later calculated as the arithmetic mean of measured body temperatures (Pough and Gans, 1982). Standard deviations of body temperatures (SD) were also calculated. Thus, lizards with high SD have low precision of thermoregulation (Paranjpe et al., 2013). Maximum and minimum body temperatures of each individual were also registered as measures of voluntarily selected temperatures (Tmax.v, and Tmin.v). In addition to these measurements of thermal preference, we also investigated the parasitic infections of these lizards. Tick load was quantified within the first day of capture and at day 11 by the same person (RM-P). In addition, following the methods described in Megía-Palma et al. (2018), the same person (RM-P) diagnosed chronic infections by hematic (i.e., Lankesterella occidentalis) and intestinal (i.e., Acroeimeria sceloporis) coccidians only once at the beginning of the trials.THIS DATASET IS ARCHIVED AT DANS/EASY, BUT NOT ACCESSIBLE HERE. TO VIEW A LIST OF FILES AND ACCESS THE FILES IN THIS DATASET CLICK ON THE DOI-LINK ABOV

Lizard host abundances and climatic factors explain phylogenetic diversity and prevalence of blood parasites on an oceanic island

1. Host abundance might favour the maintenance of a high phylogenetic diversity of some parasites via rapid transmission rates. Blood parasites of insular lizards represent a good model to test this hypothesis because these parasites can be particularly prevalent in islands and host lizards highly abundant.2. We applied deep amplicon sequencing and analysed environmental predictors of blood parasite prevalence and phylogenetic diversity in the endemic lizard Gallotia galloti across 24 localities on Tenerife, an island in the Canary archipelago that has experienced increasing warming and drought in recent years.3. Parasite prevalence assessed by microscopy was over 94% and a higher proportion of infected lizards was found in warmer and drier locations. A total of 33 different 18s rRNA parasite haplotype were identified and the phylogenetic analyses indicated that they belong to two genera of Adeleorina (Apicomplexa: Coccidia), with Karyolysus as the dominant genus. The most important predictor of between-locality variation in parasite phylogenetic diversity was the abundance of lizard hosts. 4. A combination of climatic and host demographic factors associated with an insular syndrome may be favouring a rapid transmission of blood parasites among lizards on Tenerife, which may favour the maintenance of a high phylogenetic diversity of parasites.THIS DATASET IS ARCHIVED AT DANS/EASY, BUT NOT ACCESSIBLE HERE. TO VIEW A LIST OF FILES AND ACCESS THE FILES IN THIS DATASET CLICK ON THE DOI-LINK ABOV

Natural parasites, rival’s color, and rival’s behavior explain aggression in a lizard

Male competition conforms to a cost-benefit model because aggression may increase reproductive prospects while increasing risks of injuries. We hypothesize that these agonistic interactions can also incur in energetic trade-offs in parasitized hosts. We staged dyadic male contests in the lab to investigate the relationships of multiple parasites with the agonistic behavior of lizard hosts, Sceloporus occidentalis. We also included in the analyses both color and behavioral traits from rivals because (i) color patches of lizards may serve as intraspecific signals used by conspecifics to assess the quality of opponents, and (ii) contests between male lizards fit classical models of escalated aggression, where focal lizards increase aggression displays in response to a rival’s behavior. Based on multimodel inference applied to mixed models, lizards displayed more pushups when they had more ticks and also when rivals performed more lateral compressions. The higher aggression in infested lizards might be explained as a correlate of host reproductive effort. Moreover, lizards infected by hematic coccidians performed fewer pushups, conforming to our initial hypothesis. Interestingly, focal lizards also displayed fewer pushups when the chroma and size of rival’s blue patch were greater. The results support the role of the blue patch of S. occidentalis as a sexual armament, because it contributes to the deterrence of aggression from rivals. They also revealed that natural infections in lizard hosts can contribute to explain their agonistic behavior. We encourage to account for natural infections in behavioral tests with lizards.THIS DATASET IS ARCHIVED AT DANS/EASY, BUT NOT ACCESSIBLE HERE. TO VIEW A LIST OF FILES AND ACCESS THE FILES IN THIS DATASET CLICK ON THE DOI-LINK ABOV

Genetic diversity, phylogenetic position, and co-phylogenetic relationships of Karyolysus, a common blood parasite of lizards in the Western Mediterranean

The genus Karyolysus Labbé, 1894 was originally proposed to accommodate blood parasites of lacertid lizards in Western Europe. However, recent phylogenetic analyses suggested an inconclusive taxonomic position of these parasites of the order Adeleorina based on the available genetic information. Inconsistencies between molecular phylogeny, morphology, and/or life cycles can reflect lack of enough genetic information of the target group. We therefore surveyed 28 localities and collected blood samples from 828 lizards of 23 species including lacertids, skinks, and geckoes in the Western Mediterranean, North Africa, and Macaronesia, where species of Karyolysus and other adeleorine parasites have been described. We combined molecular and microscopic methods to analyze the samples, including those from the host type species and the type locality of Karyolysus bicapsulatus. The phylogenetic relationship of these parasites was analyzed based on the 18S rRNA gene and the co-phylogenetic relationship with their vertebrate hosts was reconstructed. We molecularly detected adeleorine parasites in 37.9% of the blood samples and found 22 new parasite haplotypes. A phylogenetic reconstruction with 132 sequences indicated that 20 of the newly detected haplotypes clustered in a well-supported clade with another 18 sequences that included Karyolysus galloti and Karyolysus lacazei. Morphological evidence also supported that Karyolysus bicapsulatus clustered in this monophyletic clade. These results supported the taxonomic validity of the genus. In addition, we found some parasite haplotypes that infected different lizard host genera with ancient diverging histories, which suggested that Karyolysus is less host-specific than other blood parasites of lizards in the region. A co-phylogenetic analysis supported this interpretation because no significant co-speciation signal was evidenced between Karyolysus and lizard hosts.THIS DATASET IS ARCHIVED AT DANS/EASY, BUT NOT ACCESSIBLE HERE. TO VIEW A LIST OF FILES AND ACCESS THE FILES IN THIS DATASET CLICK ON THE DOI-LINK ABOV

Differential recovery ability from infections by two blood parasite genera in males of a Mediterranean lacertid lizard after an experimental translocation

Different blood parasites can co-infect natural populations of lizards. However, our knowledge on the host’s ability to recover from them (i.e., significantly reduce parasitaemia levels) is scarce. This has interest from an ecological immunology perspective. Herein, we investigate the host recovery ability in males of Psammodromus algirus infected by parasite genera Schellackia and Karyolysus. The role of lizard hosts is dissimilar in the life cycle of these two parasites, and thus different immune control of reproduction cycles by the vertebrate hosts is expected. As Schellackia performs both sexual and asexual reproduction cycles in lizards, we expect a better immune control by its vertebrate hosts. On the contrary, Karyolysus performs sexual reproductive cycles in vectors, hence we expect lower immune control by the lizards. We carried out a reciprocal translocation experiment during the lizards’ mating season to evaluate both parasitaemia and leukocyte profiles in male lizards, being one of the sampling plots close to a road with moderate traffic. These circumstances provide a combination of extrinsic (environmental stress) and intrinsic factors (reproductive versus immune trade-offs) that may influence host’s recovery ability. We recaptured 33% of the lizards, with a similar proportion in control and translocated groups. Karyolysus infected 92.3% and Schellackia 38.5% of these lizards. Hosts demonstrated ability to significantly reduce parasitaemia of Schellackia but not of Karyolysus. This suggests, in line with our predictions, a differential immune relationship of lizards with these parasites, at time that supports that parasites with different phylogenetic origins should be analysed separately in investigations of their effects on hosts. Furthermore, lizards close to the road underwent a stronger upregulation of lymphocytes and monocytes when translocated far from the road, suggesting a putative greater exposure to pathogens in the latter area.THIS DATASET IS ARCHIVED AT DANS/EASY, BUT NOT ACCESSIBLE HERE. TO VIEW A LIST OF FILES AND ACCESS THE FILES IN THIS DATASET CLICK ON THE DOI-LINK ABOV

To cool or not to cool? Intestinal coccidians disrupt the behavioral hypothermia of lizards in response to tick infestation

It is generally accepted that parasites exert negative effects on their hosts and that natural selection favors specific host responses that mitigate this impact. It is also known that some components of the host immune system often co-evolve with parasite antigens resulting in a host-parasite arms race. In addition to immunological components of the anti-parasitic response, host behavioral responses are also important in this arms race and natural selection may favor avoidance strategies that preclude contact with parasites, or shifts in the host's thermoregulatory strategy to combat active infections (e.g., behavioral fever). Ticks are widespread parasites with direct and indirect costs on their vertebrate hosts. Their saliva provokes hemolysis in the blood of their hosts and can transmit a plethora of tick-borne pathogens. We enquired whether tick infestation by Ixodes pacificus can provoke a thermoregulatory response in Sceloporus occidentalis. For this, we compared the thermoregulatory behavior of tick-infested lizards against tick-infested lizards co-infected with two different species of coccidians (Lankesterella occidentalis and Acroeimeria sceloporis). After this, lizards were kept in individual terraria with a basking spot and fed ad libitum. We found that tick-infested lizards sought cooler temperatures in proportion to their tick load, and this response was independent of the co-infection status by L. occidentalis. This was consistent in April and June (when tick loads were significantly lower) and suggests a conservative strategy to save energy which might have been selected to overcome tick infestations during phenological peaks of this parasite. However, this behavior was not observed in lizards co-infected with A. sceloporis, suggesting that co-infection with this intestinal parasite prompt lizards to be active. Cost of tick infestation was confirmed because housed lizards lost weight at a constant ratio to initial tick load, independently of other infections. The broader implications of these findings are discussed in the context of climate change.Research at UCSC was supported by an NSF grant (EF-1241848 to BS). Spanish Ministerio de Economía y Competitividad provided support (BES-2010-038427 and EEBB-I-14-08326 to RM-P)

Plasticity of haemoglobin concentration and thermoregulation in a mountain lizard

The plastic capability of species to cope with the new conditions created by climate change is poorly understood. This is particularly relevant for organisms restricted to high elevations because they are adapted to cold temperatures and low oxygen availability. Therefore, evaluating trait plasticity of mountain specialists is fundamental to understand their vulnerability to environmental change. We transplanted mountain lizards, Iberolacerta cyreni, 800 m downhill to evaluate the plastic response in body condition, thermoregulation traits, haemoglobin level, and haemoparasite load. Initial measurements of body mass, total haemoglobin concentration ([Hb]), hematic parasite intensities, dorsal luminance, and thermoregulatory behaviour were resampled after two and four weeks of acclimation. We also tested whether an anti-parasitic drug reduced haemoparasite intensity. After only two weeks of acclimation to a lower elevation, lizards decreased 42% in [Hb], had 17% less parasite intensities, increased body condition by 25%, and raised by ~3% their mean preferred temperatures and their voluntary thermal maximum. The anti-parasitic treatment had no significant effect on the intensity of hematic parasites, but our results suggest that negative effects of haemoparasites on [Hb] are relaxed at lower elevation. The rapid plastic changes observed in thermal preferences, body condition, [Hb], and parasite intensity of I. cyreni demonstrate a potential plastic response of a mountain specialist. This may be adaptive under the climatic extremes typical of mountain habitats. However, there is uncertainty in whether the observed plasticity can also help overcome long term environmental changes.This study was funded by projects CGL2011-30393 (PI: I. De la Riva), CGL2012-40026-384 C02-02 and PGC2018-097426-B-C21 (MINECO/ FEDER) (PI: Santiago Merino, MNCN-CSIC)

Geographic patterns of stress in insular lizards reveal anthropogenic and climatic signatures

Anthropization of insular ecosystems may have negative impacts on native populations of lizards, which provide core ecosystem services on islands. We aimed to identify environmental factors to explain the interlocal variation in faecal glucocorticoids, parasite intensity, and body condition in populations of insular lizards. A cross-sectional design during the summer of 2017 and 2018 was used to sample 611 adult lizards, Gallotia galloti. Interlocal variation of three stress indicators was analysed in response to environmental variables across a wide environmental gradient in Tenerife (Canary Islands): (i) concentration of faecal glucocorticoids, (ii) intensities of infection by hematic parasites, and (iii) body condition. The data, with low spatial autocorrelation, were analysed using multimodel inference and model cross-validation. Bioclimatic variables associated with the extreme hot and dry climate of summer were the most informative predictors. Interlocal variation in faecal corticosterone in males was best fitted to a model that included the maximum temperature of the warmest month, although the best predictor was habitat anthropization. The thermal annual range, associated with extreme thermal events, was positively related to faecal corticosterone in females. Extreme hot temperatures were positively related to the median parasite intensities in both sexes, while the highest mean intensities of infection were found in females from the most xeric coastal localities. None of the predictors tested, including faecal glucocorticoids, explained individual or interlocal variation in body condition. Effects of human pressure and climate change on insular populations of lizards can be additive. However, the uncoupled relationship found between body condition and the faecal glucocorticoid content suggests that current negative effects may be aggravated during drought periods in summer. Given the impact of climate change on islands, our results may be of application to other archipelagos, where lizards also play key ecological roles.This work was supported by research grants MINECO/FEDER (CGL2015-67789-C2-1-P to SM), FCT/FEDER (28014 02/SAICT/2017 to MAC), and state budget by the Slovenian Research Agency (ARRS, Programme P1-0255 to AŽ). RMP enjoys a postdoctoral contract (CEECIND/04084/2017) by ICETA–Instituto de Ciências, Tecnologias e Agroambiente da Universidade do Porto and Fundação da Ciência eTecnologia

Multiple color patches and parasites in Sceloporus occidentalis: Differential relationships by sex and infection

Parasites generally have a negative influence on the color expression of their hosts. Sexual selection theory predicts resistant high-quality individuals should show intense coloration, whereas susceptible low-quality individuals would show poor coloration. However, intensely colored males of different species of Old and New World lizards were more often infected by hemoparasites. These results suggest that high-quality males, with intense coloration, would suffer higher susceptibility to hemoparasites. This hypothesis remains poorly understood and contradicts general theories on sexual selection. We surveyed a population of Sceloporus occidentalis for parasites and found infections by the parasite genera Lankesterella and Acroeimeria. In this population, both males and females express ventral blue and yellow color patches. Lankesterella was almost exclusively infecting males. The body size of the males significantly predicted the coloration of both blue and yellow patches. Larger males showed darker (lower lightness) blue ventral patches and more saturated yellow patches that were also orange-skewed. Moreover, these males were more often infected by Lankesterella than smaller males. The intestinal parasite Acroeimeria infected both males and females. The infection by intestinal parasites of the genus Acroeimeria was the best predictor for the chroma in the blue patch of the males and for hue in the yellow patch of the females. Those males infected by Acroeimeria expressed blue patches with significantly lower chroma than the uninfected males. However, the hue of the yellow patch was not significantly different between infected and uninfected females. These results suggest a different effect of Lankesterella and Acroeimeria on the lizards. On the one hand, the intense coloration of male lizards infected by Lankesterella suggested high-quality male lizards may tolerate it. On the other hand, the low chroma of the blue coloration of the infected males suggested that this coloration could honestly express the infection by Acroeimeria.Ministerio de Economía, Comercio y Empres