Rodrigo Megía-Palma

Molecular characterization of haemococcidia genus Schellackia (Apicomplexa) reveals the polyphyletic origin of the family Lankesterellidae

The current taxonomy on the haemococcidia establishes that the two genera of protozoan parasites that integrate the family Lankesterellidae are Lankesterella and Schellackia. However, the phylogeny of these genera, as well as the other coccidia, remains unresolved. In this sense, the use of type and described species is essential for the resolution of systematic conflicts. In this study, we molecularly characterize the type species of the genus Schellackia, that is, S. bolivari from Europe and also a described species of the same genus from Asia. At the same time, we contribute with the molecular characterization of another species of the genus Lankesterella. All this put together supports the polyphyly of the family Lankesterellidae. Therefore, we propose the resurrection of the zoological family, Schellackiidae Grassé , to include species within the genus Schellackia.

Phylogeny of the reptilian Eimeria: are Choleoeimeria and Acroeimeria valid generic names?

Reptiles are the animals with the most described coccidian species among all vertebrates. However, the co‐evolutionary relationships in this host–parasite system have been scarcely studied. Paperna & Landsberg (South African Journal of Zoology, 24, 1989, 345) proposed the independent evolutionary origin of the Eimeria‐like species isolated from reptiles based on morphological and developmental characteristics of their oocysts. Accordingly, they suggested the reclassification of these parasites in two new genera, Choleoeimeria and Acroeimeria. The validity of the genera proposed to classify reptilian Eimeria species remained unresolved due to the lack of species genetically characterized. In this study, we included 18S rRNA gene sequences from seven Eimeria‐like species isolated from five different lizard host families. The phylogenetic analyses confirmed the independent evolutionary origin of the Eimeria‐like species infecting lizards. Within this group, most species were placed into two monophyletic clades. One of them included the species with ellipsoidal oocysts (i.e. Choleoeimeria‐like oocysts), whereas the species with more spheroidal oocysts (i.e. Acroeimeria‐like oocysts) were included in the second one. This result supports the taxonomic validity of the genera Acroeimeria and Choleoeimeria.

Phylogenetic relationships of Isospora, Lankesterella, and Caryospora species (Apicomplexa: Eimeriidae) infecting lizards

In this study, several species of Isospora infecting lizards were genetically characterized. Specifically, five described and four newly described species of Isospora were included in a phylogeny of the family Eimeriidae. These species were isolated from hosts originally inhabiting all geographic continents except Europe. Phylogenetic analyses of the 18S ribosomal RNA (rRNA) gene grouped these nine species of Isospora with Lankesterella species and Caryospora ernsti. Therefore, within this clade, different evolutionary strategies in oocyst development and transmission occurred. Although the characteristic endogenous oocyst development of the genus Lankesterella may have arisen only once, the reduction in the number of sporocysts observed in the genus Caryospora occurred at least twice during coccidian evolution, as evidenced by the phylogenetic position of Caryospora bigenetica as the sister taxon of the group formed by reptilian Isospora, Lankesterella, and C. ernsti. Within this group, C. ernsti was the sister taxon to the genus Lankesterella. Overall, our results contradict the proposed monophyly of the genus Caryospora, highlighting the need for a thorough taxonomic and systematic revision of the group. Furthermore, they suggest that the recent ancestor of the genus Lankesterella may have been heteroxenous.

Manipulation of parasite load induces significant changes in the structural-based throat color of male iberian green lizards

Abstract The honesty of structural-based ornaments is controversial. Sexual selection theory predicts that the honesty of a sexual signal relies on its cost of production or maintenance. Therefore, environmental factors with negative impact on individuals could generate high costs and affect the expression of these sexual signals. In this sense, parasites are a main cost for their hosts. To probe the effect of parasites on the structural-based coloration of a lacertid species Lacerta schreiberi, we have experimentally removed ticks from a group of male Iberian green lizards using an acaricide treatment (i.e., the broad-use insecticide fipronil). All individuals were radio-tracked and recaptured after 15 days to study changes in coloration in both the ultraviolet (UV)-blue (structural-based) and UV-yellow (structural and pigment-based) ornamentations after manipulation, as well as changes in endo- and ectoparasitic load and body condition. Additionally, after the experiment, we measured the skin inflammatory response to a mitogen. The fipronil treatment was effective in reducing ticks and it was associated with a significant reduction of hemoparasite load. Throughout the season, individuals treated with fipronil tended to maintain the brightness of the UV-blue throat coloration while control lizards tended to increase it. However, individuals treated with fipronil that were not infected with hemoparasites significantly reduced the brightness of the UV-blue throat coloration. Individuals with a higher initial tick load exhibited a lower UV saturation increment (UV-blue) and a higher brightness increment (UV-yellow) during the experiment. Overall these results experimentally support the idea that parasites adversely influence the expression of the structural-based coloration of male Iberian green lizards. This adds evidence to the hypothesis that sexual ornaments in lizards function as honest signals.

Opposed elevational variation in prevalence and intensity of endoparasites and their vectors in a lizard

Abstract Studying the causes of parasite geographic distribution is relevant to understand ecological and evolutionary processes that affect host populations as well as for species conservation. Temperature is one of the most important environmental variables affecting parasite distribution, as raising temperatures positively affect development, reproduction, and rate of transmission of both endo- and ectoparasites. In this context, it is generally accepted that, in mountains, parasite abundance decreases with elevation. However, empirical evidence on this topic is limited. In the present study, we analyzed the elevational variation of hemoparasites and ectoparasites of a lizard, Psammodromus algirus, along a 2,200-m elevational gradient in Sierra Nevada (SE Spain). As predicted, ectoparasite (mites, ticks, mosquitoes, and sandflies) abundance decreased with elevation. However, hemoparasite prevalence and intensity in the lizard augmented with altitude, showing a pattern contrary to their vectors (mites). We suggest that tolerance to hemoparasites may increase with elevation as a consequence of lizards at high altitudes taking advantage of increased body condition and food availability, and reduced oxidative stress. Moreover, lizards could have been selected for higher resistance against hemoparasites at lowlands (where higher rates of replication are expected), thus reducing hemoparasite prevalence and load. Our findings imply that, in a scenario of climate warming, populations of lizards at high elevation may face increased abundance of ectoparasites, accompanied with strong negative effects.

Interpopulational and seasonal variation in the chemical signals of the lizard Gallotia galloti

Communicative traits are strikingly diverse and may vary among populations of the same species. Within a population, these traits may also display seasonal variation. Chemical signals play a key role in the communication of many taxa. However, we still know far too little about chemical communication in some vertebrate groups. In lizards, only a few studies have examined interpopulational variation in the composition of chemical cues and signals and only one study has explored the seasonal effects. Here we sampled three subspecies of the Tenerife lizards (Gallotia galloti) and analyze the lipophilic fraction of their femoral gland secretions to characterize the potential interpopulational variation in the chemical signals. In addition, we assessed whether composition of these secretions differed between the reproductive and the non-reproductive season. We analyzed variations in both the overall chemical profile and the abundance of the two main compounds (cholesterol and vitamin E). Our results show interpopulational and seasonal differences in G. gallotia chemical profiles. These findings are in accordance with the high interpopulational variability of compounds observed in lizard chemical signals and show that their composition is not only shaped by selective factors linked to reproductive season.

Phylogenetic analyses reveal that Schellackia parasites (Apicomplexa) detected in American lizards are closely related to the genus Lankesterella: is the range of Schellackia restricted to the Old World?

BackgroundSpecies of Schellackia Reichenow, 1919 have been described from the blood of reptiles distributed worldwide. Recently, Schellackia spp. detected in European and Asian lizards have been molecularly characterised. However, parasites detected in American lizard hosts remain uncharacterised. Thus, phylogenetic affinities between the Old and New World parasite species are unknown.MethodsIn the present study, we characterised morphologically and molecularly the hemococcidian parasites (sporozoites) that infect three lizard hosts from North America and two from South America.ResultsIn total, we generated 12 new 18S rRNA gene sequences of hemococcidian parasites infecting New World lizard hosts. By the microscopic examination of the smears we identified Schellackia golvani Rogier & Landau, 1975 (ex Anolis carolinensis Voigt) and Schellackia occidentalis Bonorris & Ball, 1955 (ex Uta stansburiana Baird & Girard and Sceloporus occidentalis Baird & Girard) in some samples, but the phylogenetic analysis indicated that all 18S rDNA sequences are distant from Schellackia species found in Old World lizards. In fact, the hemococcidian parasites detected in the New World lizards (including S. occidentalis and S. golvani) were closely related to the genus Lankesterella Labbé, 1899. Consequently, we suggest these two species to be included within the genus Lankesterella.ConclusionsLife history traits of hemococcidian parasites such as the type of host blood cells infected, host species or number of refractile bodies are not valid diagnostic characteristics to differentiate the parasites between the genera Schellackia and Lankesterella. Indeed, lankesterellid parasites with a different number of refractile bodies had a close phylogenetic origin. Based on the phylogenetic results we provide a systematic revision of the North American hemococcidians. Our recommendation is to include the species formerly described in the genus Schellackia that infect American lizards into Lankesterella (Lankesterellidae) as Lankesterella golvani (Rogier & Landau, 1975) n. comb and L. occidentalis (Bonorris & Ball, 1955) n. comb.

Raman Spectroscopy Reveals the Presence of Both Eumelanin and Pheomelanin in the Skin of Lacertids

Abstract Melanic pigments play a key role in the coloration of animals, but the type of melanin pigment in black, brown, and blue colored scales of Squamata has not been studied. Based on research on birds and mammals, we may expect that pheomelanin is the majority pigment in brownish colorations and eumelanin is the majority pigment in black and blue colorations of Squamata. To characterize the pigments that underlie the melanin-based colorations of lizards, we analyzed the skin of nine genera of lacertids using dispersive Raman spectroscopy. Our results suggest that no prediction can be made on the type of pigmentary melanin present in the skin of the lacertids based alone on the hue of the sample. Indeed, brownish patterns in the skin of Psammodromus, Gallotia, Acanthodactylus, and Algyroides lizards presented both chemical forms of melanin: eumelanin and pheomelanin. Therefore, pheomelanogenesis might be an ancient characteristic within Lacertidae, because it was detected in genera in the Lacertini, Eremini, and Gallotini. Raman spectra of melanic-based patterns of genus Zootoca and ultraviolet (UV)-blue patches of Podarcis, Iberolacerta, Lacerta, and Timon lizards suggested that eumelanin is the majority pigment in these patches. Raman spectroscopy is a suitable nondestructive technique useful to identify melanin forms in the skin of lizards, and it demonstrated that pheomelanin is synthesized by Squamata. Resumen Los pigmentos melánicos juegan un papel clave en la coloración de los animales. Sin embargo, en los Squamata se desconoce la identidad molecular de los pigmentos melánicos (i.e., eumelanina y feomelanina) responsables de las coloraciones negras, marrones y azules. Basado en estudios anteriores en aves y mamíferos, cabría esperar que la feomelanina fuera el pigmento mayoritario en coloraciones marrones y que la eumelanina sea el pigmento mayoritario en las coloraciones negras y azules de los Squamata. Para caracterizar los pigmentos responsables de la coloración melánica en lagartos hemos analizado la piel de nueve géneros de lacértidos usando espectroscopía Raman dispersiva. Nuestros resultados sugieren que no se puede predecir el tipo de melanina pigmentaria presente en la piel de los lácertidos basándonos solo en la tonalidad de la muestra. De hecho, en los patrones de color marrón de la piel de lagartos de los géneros Psammodromus, Gallotia, Acanthodactylus y Algyroides están presentes ambas formas químicas de la melanina pigmentaria, es decir, eumelanina y feomelanina. En los patrones melánicos del género Zootoca y en las manchas ultravioleta (UV)-azules de lagartos en los géneros Podarcis, Iberolacerta, Lacerta, y Timon el espectro Raman sugirió que la forma eumelánica debe de ser el pigmento mayoritario en estas manchas. La espectroscopía Raman es una técnica no destructiva que es aplicable para identificar las formas melánicas presentes en la piel de los lagartos y demostró que los Squamata pueden sintetizar feomelanina.

Molecular evidence for host–parasite co-speciation between lizards and Schellackia parasites

Current and past parasite transmission may depend on the overlap of host distributions, potentially affecting parasite specificity and co-evolutionary processes. Nonetheless, parasite diversification may take place in sympatry when parasites are transmitted by vectors with low mobility. Here, we test the co-speciation hypothesis between lizard final hosts of the Family Lacertidae, and blood parasites of the genus Schellackia, which are potentially transmitted by haematophagous mites. The effects of current distributional overlap of host species on parasite specificity are also investigated. We sampled 27 localities on the Iberian Peninsula and three in northern Africa, and collected blood samples from 981 individual lizards of seven genera and 18 species. The overall prevalence of infection by parasites of the genus Schellackia was ∼35%. We detected 16 Schellackia haplotypes of the 18S rRNA gene, revealing that the genus Schellackia is more diverse than previously thought. Phylogenetic analyses showed that Schellackia haplotypes grouped into two main monophyletic clades, the first including those detected in host species endemic to the Mediterranean region and the second those detected in host genera Acanthodactylus, Zootoca and Takydromus. All but one of the Schellackia haplotypes exhibited a high degree of host specificity at the generic level and 78.5% of them exclusively infected single host species. Some host species within the genera Podarcis (six species) and Iberolacerta (two species) were infected by three non-specific haplotypes of Schellackia, suggesting that host switching might have positively influenced past diversification of the genus. However, the results supported the idea that current host switching is rare because there existed a significant positive correlation between the number of exclusive parasite haplotypes and the number of host species with current sympatric distribution. This result, together with significant support for host-parasite molecular co-speciation, suggests that parasites of the genus Schellackia co-evolved with their lizard hosts.

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

Abstract 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.