Do sexual differences in life strategies make male lizards more susceptible to parasite infection?

Female and male hosts may maximise their fitness by evolving different strategies to compensate for the costs of parasite infections. The resulting sexual dimorphism might be apparent in differential relationships between parasite load and body condition, potentially reflecting differences in energy allocation to anti-parasitic defences. For example, male lacertids with high body condition may produce many offspring while being intensely parasitised. In contrast, female lacertids may show a different outcome of the trade-offs between body condition and immunity, aiming to better protect themselves from the harm of parasites. We predicted that females would have fewer parasites than males and a lower body condition across parasitaemia levels because they would invest resources in parasite defence to mitigate the costs of infection. In contrast, the male strategy to maximise access to females would imply some level of parasite tolerance and, thus, higher parasitaemia. We analysed the relationship between the body condition of lizards and the parasitemias of Karyolysus and Schellackia, two genera of blood parasites with different phylogenetic origins, in 565 females and 899 males belonging to 10 species of the Lacertidae (Squamata). These lizards were sampled over a period of 12 years across 34 sampling sites in southwestern Europe. The results concerning the Karyolysus infections were consistent with the predictions, with males having similar body condition across parasitaemia levels even though they had higher infection intensities than females. On the other hand, females with higher levels of Karyolysus parasitaemia had lower body condition. This is consistent with the prediction that different life strategies of male and female lacertids can explain the infection patterns of Karyolysus. In contrast, the parasitaemia of Schellackia was consistently low in both male and female hosts, with no significant effect on the body condition of lizards. This suggests that lizards of both sexes maintain this parasite below a pathogenic threshold.

Los machos y hembras pueden maximizar su eficacia biológica mediante la evolución diferencial de estrategias que compensen los costes asociados con las infecciones parasitarias. Por ejemplo, los machos con una alta condición corporal pueden producir muchas crías aun estando altamente parasitados. Mientras que es común que las hembras inviertan más energía en protegerse frente a los parásitos, lo que podría comprometer el mantenimiento de su condición corporal. Nuestra hipótesis es que las diferencias sexuales en la asignación de energía pueden quedar de manifiesto al analizar la relación entre la intensidad de infección con la condición corporal. También esperamos que las hembras tengan menos parásitos que los machos y que su condición corporal esté correlacionada negativamente con su carga parasitaria. Por el contrario, esperamos que los machos tengan más parásitos en parte porque su estrategia implicaría cierto nivel de tolerancia si con ello pueden incrementar su inversión reproductiva. Hemos analizado la relación entre la condición corporal y las parasitemias de Schellackia y Karyolysus, dos parásitos sanguíneos, en 565 hembras y 899 machos de 10 especies de la familia Lacertidae (Squamata) durante 12 años en 34 localidades en el suroeste de Europa. El patrón para Karyolysus fue coherente con las predicciones, ya que la condición corporal de los machos no se correlacionó con su parasitemia, a pesar de que estas fueron mayores que en las hembras. Mientras que la relación fue negativa en las hembras. Por lo que el patrón de infección de Karyolysus concuerda con las diferentes estrategias de inversión energética en machos y hembras. Sin embargo, en el caso de Schellackia las parasitemias fueron más bajas en hospedadores de ambos sexos y su parasitemia no se correlacionó con la condición corporal. Este resultado sugiere que Schellackia es mantenido en umbrales subpatogénicos.

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

The genus Karyolysus 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 K. 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 shown between Karyolysus and lizard hosts.

Sexual selection, feather wear, and time constraints on the pre-basic molt explain the acquisition of the pre-alternate molt in European passerines.

Avian feathers need to be replaced periodically to fulfill their functions, with natural, social, and sexual selection presumably driving the evolution of molting strategies. In temperate birds, a common pattern is to molt feathers immediately after the breeding season, the pre-basic molt. However, some species undergo another molt in winter-spring, the pre-alternate molt. Using a sample of 188 European passerine species, Bayesian phylogenetic mixed models, and correlated evolution analyses, we tested whether the occurrence of the pre-alternate molt was positively associated with proxies for sexual selection (sexual selection hypothesis) and nonsexual social selection (social selection hypothesis), and with factors related to feather wear (feather wear hypothesis) and time constraints on the pre-basic molt (time constraints hypothesis). We found that the pre-alternate molt was more frequent in migratory and less gregarious species inhabiting open/xeric habitats and feeding on the wing, and marginally more frequent in species with strong sexual selection and those showing a winter territorial behavior. Moreover, an increase in migratory behavior and sexual selection intensity preceded the acquisition of the pre-alternate molt. These results provide support for the feather wear hypothesis, partial support for the sexual selection and time constraints hypotheses, and no support for the social selection hypothesis.

Hormonal control of seasonal color change in female spiny-footed lizards: an observational and experimental approach.

Breeding coloration of females often signals aspects of their reproductive status, suggesting a link between color and sex steroid hormones. In this study, we examined the relationships between 2 sex steroid hormones (progesterone and ß-estradiol) and reproductive coloration in female spiny-footed lizards Acanthodactylus erythrurus. We first explored natural variation in female plasma hormone levels and coloration during their reproductive cycle. ß-estradiol was negatively related to brightness and positively related to red saturation, whereas progesterone was not significantly related to coloration. After identifying key relationships, plasma hormone concentrations were manipulated by creating 3 experimental female groups (ß-estradiol-treated, progesterone-treated, and control), and the effects on coloration were monitored. ß-estradiol-treated females, in which there was a rise in both ß-estradiol and progesterone levels, lost their red coloration earlier than females in the other 2 experimental groups, whereas progesterone treatment had no significant effect on female coloration. Our results suggest that high levels of either ß-estradiol alone or ß-estradiol together with progesterone trigger the loss of red coloration in female spiny-footed lizards, and that progesterone alone does not affect coloration. We hypothesize that changes in female breeding color might be regulated by ß-estradiol in species in which conspicuous coloration is displayed before ovulation, and by progesterone in species in which this color is displayed during gravidity.

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.

Colonial, more widely distributed and less abundant bird species undergo wider population fluctuations independent of their population trend.

Understanding temporal variability in population size is important for conservation biology because wide population fluctuations increase the risk of extinction. Previous studies suggested that certain ecological, demographic, life-history and genetic characteristics of species might be related to the degree of their population fluctuations. We checked whether that was the case in a large sample of 231 European breeding bird species while taking a number of potentially confounding factors such as population trends or similarities among species due to common descent into account. When species-specific characteristics were analysed one by one, the magnitude of population fluctuations was positively related to coloniality, habitat, total breeding range, heterogeneity of breeding distribution and natal dispersal, and negatively related to urbanisation, abundance, relative number of subspecies, parasitism and proportion of polymorphic loci. However, when abundance (population size) was included in the analyses of the other parameters, only coloniality, habitat, total breeding range and abundance remained significantly related to population fluctuations. The analysis including all these predictors simultaneously showed that population size fluctuated more in colonial, less abundant species with larger breeding ranges. Other parameters seemed to be related to population fluctuations only because of their association with abundance or coloniality. The unexpected positive relationship between population fluctuations and total breeding range did not seem to be mediated by abundance. The link between population fluctuations and coloniality suggests a previously unrecognized cost of coloniality. The negative relationship between population size and population fluctuations might be explained by at least three types of non-mutually exclusive stochastic processes: demographic, environmental and genetic stochasticity. Measurement error in population indices, which was unknown, may have contributed to the negative relationship between population size and fluctuations, but apparently only to a minor extent. The association between population size and fluctuations suggests that populations might be stabilized by increasing population size.

MODE OF ATTACHMENT AND PATHOLOGY CAUSED BY PARORCHITES ZEDERI IN THREE SPECIES OF PENGUINS: PYGOSCELIS PAPUA, PYGOSCELIS ADELIAE, AND PYGOSCELIS ANTARCTICA IN ANTARCTICA.

We identified and compared gross and microscopic lesions associated with the cestode, Parorchites zederi, in the digestive tracts of three species of penguins (Spheniscidae): the Chinstrap ( Pygoscelis antarctica ), Gentoo ( Pygoscelis papua ), and Adélie penguins ( Pygoscelis adeliae ). The gastrointestinal tracts of 79 recently dead individuals (71 chicks and eight adults) were collected in locations throughout the Antarctic Peninsula during summer field trips in 2006-09. Parorchites zederi was found in the small intestine of 37 animals (47%), and 23 (62%) of these had parasite-associated lesions. The cestodes were either free in the intestinal lumen, clustered within mucosal ulcers, or deeply embedded in the intestinal wall. Histopathologic changes were most severe in adult Gentoo Penguins and included transmural fibrogranulomatous enteritis, hemorrhage, and edema. This report of pathology associated with P. zederi in the digestive tracts of penguins can serve as reference to monitor health in Antarctic birds associated with environmental changes.

Coloration reflects skin pterin concentration in a red-tailed lizard.

When integumentary tissue pigments are contained in chromatophores, tissue color might not depend exclusively on the amount of pigment. Whether coloration does or does not reflect pigment concentration may be very significant for intraspecific communication, for example when pigment concentration provides fitness-related information. We studied the pigment responsible for the orange/red ventral tail coloring in a lacertid lizard species (Acanthodactylus erythrurus), and whether the color was related to skin pigment concentration. The pigment was identified as a pterin, a higher concentration of which resulted in darker, more red-saturated, redder (less orange) ventral tail skin color. The dorsal tail integument, even though it appears mostly gray to the naked eye, also contained pterins, and furthermore, the dorsal and ventral pterin concentrations were positively correlated. A possible explanation for these results is that pterins accumulate in the skin of the whole tail, even if only needed in the ventral part, but are concealed in the dorsal part. In this way, ventral orange/red coloration would accurately reflect pterin concentration, which provides the basis for a signaling function, while dorsal coloration would become less conspicuous as an anti-predatory mechanism.

Temporal variation in population size of European bird species: effects of latitude and marginality of distribution.

In the Northern Hemisphere, global warming has been shown to affect animal populations in different ways, with southern populations in general suffering more from increased temperatures than northern populations of the same species. However, southern populations are also often marginal populations relative to the entire breeding range, and marginality may also have negative effects on populations. To disentangle the effects of latitude (possibly due to global warming) and marginality on temporal variation in population size, we investigated European breeding bird species across a latitudinal gradient. Population size estimates were regressed on years, and from these regressions we obtained the slope (a proxy for population trend) and the standard error of the estimate (SEE) (a proxy for population fluctuations). The possible relationships between marginality or latitude on one hand and slopes or SEE on the other were tested among populations within species. Potentially confounding factors such as census method, sampling effort, density-dependence, habitat fragmentation and number of sampling years were controlled statistically. Population latitude was positively related to regression slopes independent of marginality, with more positive slopes (i.e., trends) in northern than in southern populations. The degree of marginality was positively related to SEE independent of latitude, with marginal populations showing larger SEE (i.e., fluctuations) than central ones. Regression slopes were also significantly related to our estimate of density-dependence and SEE was significantly affected by the census method. These results are consistent with a scenario in which southern and northern populations of European bird species are negatively affected by marginality, with southern populations benefitting less from global warming than northern populations, thus potentially making southern populations more vulnerable to extinction.

The allometric pattern of sexually size dimorphic feather ornaments and factors affecting allometry.

The static allometry of secondary sexual characters is currently subject to debate. While some studies suggest an almost universal positive allometry for such traits, but isometry or negative allometry for nonornamental traits, other studies maintain that any kind of allometric pattern is possible. Therefore, we investigated the allometry of sexually size dimorphic feather ornaments in 67 species of birds. We also studied the allometry of female feathers homologous to male ornaments (female ornaments in the following) and ordinary nonsexual traits. Allometries were estimated as reduced major axis slopes of trait length on tarsus length. Ornamental feathers showed positive allometric slopes in both sexes, although that was not a peculiarity for ornamental feathers, because nonsexual tail feathers also showed positive allometry. Migration distance (in males) and relative size of the tail ornament (in females) tended to be negatively related to the allometric slope of tail feather ornaments, although these results were not conclusive. Finally, we found an association between mating system and allometry of tail feather ornaments, with species with more intense sexual selection showing a smaller degree of allometry of tail ornaments. This study is consistent with theoretical models that predict no specific kind of allometric pattern for sexual and nonsexual characters.

Minisatellite mutation rates increase with extra-pair paternity among birds.

BACKGROUND: Amos suggested recently that a previously reported positive relationship between minisatellite mutation rates and extra-pair paternity among species of birds was confounded by transcription errors and selective inclusion of studies. Here we attempted to replicate the results reported by Amos, but also tested for the relationship by expanding the data base by including studies published after our original paper. RESULTS: We were able to replicate the positive association between mutation rate and extra-pair paternity in birds, even after controlling statistically for the confounding effecs of mean number of bands scored, using 133 species, compared to 81 species in our first report 2. We suggest that Amos failed to reach a similar conclusion due to four different potential causes of bias. First, Amos missed 15 studies from the literature that we were able to include. Second, he used estimates of mutation rates that were based on both within- and extra-pair offspring, although the latter will cause bias in estimates. Third, he made a number of transcription errors from the original publications for extra-pair paternity, mutation rates, number of novel bands, and mean number of bands scored per individual. Fourth, he included Vireo olivaceus although the mutation rate estimate was based on one single offspring! CONCLUSION: There was a positive association between mutation rates and extra-pair paternity in birds, accounting for an intermediate effect size that explained 5-11% of the variance; estimates that are bound to be conservative due to many different causes of noise in the data. This result was robust to statistical control for potentially confounding variables, highlighting that it is important to base comparative studies on all available evidence, and that it is crucial to critically transcribe data while simultaneously checking published estimates for their correctness.

Sexually selected egg coloration in spotless starlings.

It has been recently proposed that the blue-green coloration in eggs of many avian species may constitute a sexually selected female signal. Blue-green color intensity would reflect the physiological condition of females, and hence it might also affect the allocation of male parental care. In this study, we use three different experimental approaches to explore the importance of sexual selection on blue-green egg coloration of spotless starling (Sturnus unicolor) eggs. First, experimental deterioration of female body condition (by means of wing feather removal) negatively affected the intensity of blue-green egg coloration. Second, blue-green color intensity of artificial model eggs had a significant positive influence on paternal feeding effort. Finally, we found a negative relationship between the effect of experimental food supply on nestling immunocompetence and the intensity of blue-green coloration of eggs, suggesting that egg color predicts nutritional conditions that nestlings will experience during development. All these results taken together strongly support a role of sexual selection in the blue-green coloration of spotless starling eggs.