José Miguel Aparicio

What should we weigh to estimate heterozygosity, alleles or loci?

The interest to study the effects of inbreeding in natural populations has increased in the last years. Several microsatellite‐derived metrics have recently been developed to infer inbreeding from multilocus heterozygosity data without requiring detailed pedigrees that are difficult to obtain in open populations. Internal relatedness (IR) is currently the most widespread used index and its main attribute is that allele frequency is incorporated into the measure. However, IR underestimates heterozygosity of individuals carrying rare alleles. For example, descendants of immigrants paired with natives (normally more outbred) bearing novel or rare alleles would be considered more homozygous than descendants of native parents. Thus, the analogy between homozygosity and inbreeding that generally is carried out would have no logic in those cases. We propose an alternative index, homozygosity by loci (HL) that avoids such problems by weighing the contribution of each locus to the homozygosity index depending on their allelic variability. Under a wide range of simulated scenarios, we found that our index (HL) correlated better than both IR and uncorrected homozygosity (HO), measured as proportion of homozygous loci) with genome‐wide homozygosity and inbreeding coefficients in open populations. In these populations, which are likely to prevail in nature, the use of HL instead of IR reduced considerably the sample sizes required to achieve a given statistical power. This is likely to have important consequences on the ability to detect heterozygosity fitness correlations assuming the relationship between genome‐wide heterozygosity and fitness traits.

Seasonal variation in sex ratio and sexual egg dimorphism favouring daughters in first clutches of the spotless starling

We investigated possible pre‐hatching mechanisms of sex‐differential investment by females that may contribute to offspring sex‐ratio adjustment enhancing the fitness return from reproductive effort in the spotless starling (Sturnus unicolor). We found a seasonal shift in sex ratio from daughters to sons as the season advances. Furthermore, the probability of breeding at 1‐year old and recruitment into the breeding population in daughters is associated with laying date but not with mass at fledging. The reverse is true for males which rarely bred at 1‐year old. We also found that eggs containing female embryos are significantly heavier than those containing males in spite of the slight sexual dimorphism in favour of males. This suggests maternal control of provisioning, favouring daughters that may balance sibling mortality and competition with their brothers. Our results on seasonal variation in sex ratio and differential egg provisioning are consistent with an adaptive tactic in which mothers increase their reproductive return by enhancing the probability that daughters survive and breed in their first year of life.

Sexual dimorphism in house sparrow eggs

Abstract Recent evidence has revealed an apparently high degree of control by female birds over the physiological aspects of their reproduction and offspring sex allocation, consistent with adaptive hypotheses of sex allocation and differential investment in their offspring. In the house sparrow, we investigated possible mechanisms that may be used by females to enhance the fitness returns from a reproductive effort. Using molecular techniques, we demonstrate that house sparrow eggs containing male embryos are significantly larger than those containing female embryos. We also found that male embryos were laid randomly with respect to laying order. We speculate that this sexual dimorphism of eggs is adaptive, because male house sparrows show greater variance in condition-dependent reproductive success than females. More important, the result provides further evidence of the ability of females to detect or control ovulation of either male or female ova and to differentially invest in one sex over the other.

Egg production and individual genetic diversity in lesser kestrels

Fecundity is an important component of individual fitness and has major consequences on population dynamics. Despite this, the influence of individual genetic variability on egg production traits is poorly known. Here, we use two microsatellite‐based measures, homozygosity by loci and internal relatedness, to analyse the influence of female genotypic variation at 11 highly variable microsatellite loci on both clutch size and egg volume in a wild population of lesser kestrels (Falco naumanni). Genetic diversity was associated with clutch size, with more heterozygous females laying larger clutches, and this effect was statistically independent of other nongenetic variables such as female age and laying date, which were also associated with fecundity in this species. However, egg volume was not affected by female heterozygosity, confirming previous studies from pedigree‐based breeding experiments which suggest that this trait is scarcely subjected to inbreeding depression. Finally, we explored whether the association between heterozygosity and clutch size was due to a genome‐wide effect (general effect) or to single locus heterozygosity (local effect). Two loci showed a stronger influence but the correlation was not fully explained by these two loci alone, suggesting that a main general effect underlies the association observed. Overall, our results underscore the importance of individual genetic variation for egg production in wild bird populations, a fact that could have important implications for conservation research and provides insights into the study of clutch size evolution and genetic variability maintenance in natural populations.

A test of the hypothesis of mate choice based on heterozygosity in the spotless starling

The hypothesis of mate choice based on heterozygosity predicts that sexual traits will reach their extreme expression in males with the greatest average heterozygosity, and that both a male’s ornament expression and his mating success will correlate positively with degree of individual heterozygosity. In agreement with the first prediction, we found a negative correlation between degree of homozygosity and length of the throat feathers (a secondary sexual trait) in male spotless starlings, Sturnus unicolor. However, we found a quadratic relationship between degree of homozygosity and both mating success and mean number of young sired per year. Hence, males of intermediate heterozygosity were more successful in mating and reproduction than either more homozygous or more heterozygous males. These results do not support the hypothesis of mate choice based on heterozygosity.

EFFECTS OF FOOD SUPPLEMENTATION AND HABITAT SELECTION ON TIMING OF LESSER KESTREL BREEDING

Numerous experimental studies providing extra food have concluded that food availability at the beginning of the breeding season constrains the start of egg-laying for female birds (Food Supply Hypothesis) because supplemented females usually lay earlier than nonsupplemented ones. This conclusion has recently been questioned because food addition studies may be confounded by ordered habitat selection. Ordered habitat selection occurs when territories or nests provided with extra food are chosen by individuals of higher quality that may be able to initiate breeding early, regardless of food supply (Habitat Selection Hypothesis). To test these two hypotheses, we performed an experiment using the Lesser Kestrel (Falco naumanni). To reveal effects of ordered habitat selection, extra food was provided to half of the nests in two colonies in which the other nests remained unsupplemented (mixed colonies). We provided extra food to all nests in two colonies (all-fed colonies) and to no nests in three colonies (all-unfed colonies). In these colonies, ordered habitat selection could not occur because all nests received equal treatment. In mixed colonies, fed pairs laid earlier than unfed ones. In contrast to the prediction of the Habitat Selection Hypothesis, there was no significant difference in mean laying date between unfed pairs of mixed colonies and pairs in all-unfed colonies, or between fed pairs of mixed colonies and pairs in all-fed colonies. Moreover, laying date was significantly earlier in all-fed than in all-unfed colonies. Therefore, the results support the Food Supply Hypothesis and refute the Habitat Selection Hypothesis.

THE EFFECTS OF THE MINIMUM THRESHOLD CONDITION FOR BREEDING ON OFFSPRING SEX-RATIO ADJUSTMENT IN THE LESSER KESTREL

Abstract.— We propose a model for sex‐ratio adjustment complementary to that of Trivers and Willard. In addition to the three basic assumptions of the Trivers‐Willard model, our model assumes that the sex with more variable reproductive success (normally male) is also the sex less constrained for reproduction. This assumption seems realistic, because several studies have demonstrated that poor‐condition males may adopt alternative mating strategies and sire some offspring, whereas females have physiological constraints for gestation or egg production that cannot be avoided. Thus, under these circumstances, sons of both poor and good condition would be more valuable for parents than daughters, whereas daughters would be relatively more valuable than sons at intermediate condition. This model predicts, therefore, a U‐shaped relationship between parental condition and offspring sex ratio. We present a case study for the monogamous lesser kestrel (Falco naumanni) that fulfills the assumptions and predictions of the model. The minimum body condition for breeding, measured as pectoral thickness, was lower for sons than for daughters. Below this minimum, males had a higher chance of breeding than females. Above this minimum, however, the lifetime reproductive success was condition dependent in males but not in females. Thus, males in better body condition attain, on average, higher reproductive success than females. Offspring sex ratio varied with the size of the fathers ornaments and mother condition according to the U‐shaped pattern predicted by the model.

Experimental test on public information use in the colonial Lesser Kestrel

The formation of colonies and the evolution of coloniality have been suggested to be a by-product of the use of public information to select breeding habitats. In this study we performed an experimental test to investigate whether the Lesser Kestrel (Falco naumanni) uses breeding success of conspecifics as a source of public information to select a breeding colony. We considered four potential cues based on reproductive performance of conspecifics in each colony: mean and variance of breeding success measured in both all pairs (TRS, total reproductive success), and only successful pairs (PRS, partial reproductive success). Both mean PRS and mean TRS could be predictive cues of the future reproductive output at a given site, because they varied among colonies and were autocorrelated from one year to the next. To dissociate any relationship between habitat quality and reproductive success we manipulated the mean brood sizes by transferring chicks among ten colonies. In five colonies, all the broods with at least two nestlings were reduced in one chick and in other five colonies all broods were enlarged by one chick. In the following year, we found that the number of adult immigrant kestrels settled at a colony was only explained by mean PRS in the previous year. We also examined the settlement of yearlings, which lack of information on breeding success in previous years. Unlike adult immigrant kestrels, yearlings tended to settle more frequently in those colonies with low mean PRS in the previous year, probably because of the lower pressure for occupation in those colonies. A multiple regression analysis showed that the growth of colonies was positively dependent on the mean PRS in the experimental year, and negatively on the number of predated nests. This study provides a solid support to the hypothesis that colonial species can use mean breeding success of successful pairs as a source of public information to make settlement decisions.

Risk of ectoparasitism and genetic diversity in a wild lesser kestrel population.

Parasites and infectious diseases are major determinants of population dynamics and adaptive processes, imposing fitness costs to their hosts and promoting genetic variation in natural populations. In the present study, we evaluate the role of individual genetic diversity on risk of parasitism by feather lice Degeeriella rufa in a wild lesser kestrel population (Falco naumanni). Genetic diversity at 11 microsatellite loci was associated with risk of parasitism by feather lice, with more heterozygous individuals being less likely to be parasitized, and this effect was statistically independent of other nongenetic parameters (colony size, sex, location, and year) which were also associated with lice prevalence. This relationship was nonlinear, with low and consistent prevalences among individuals showing high levels of genetic diversity that increased markedly at low levels of individual heterozygosity. This result appeared to reflect a genome‐wide effect, with no single locus contributing disproportionably to the observed effect. Thus, overall genetic variation, rather than linkage of markers to genes experiencing single‐locus heterosis, seems to be the underlying mechanism determining the association between risk of parasitism and individual genetic diversity in the study host–parasite system. However, feather lice burden was not affected by individual heterozygosity; what suggest that differences in susceptibility, rather than variation in defences once the parasite has been established, may shape the observed pattern. Overall, our results highlight the role of individual genetic diversity on risk of parasitism in wild populations, what has both important evolutionary implications and major consequences for conservation research on the light of emerging infectious diseases that may endanger genetically depauperated populations.

Increase of heterozygosity in a growing population of lesser kestrels

The lesser kestrel (Falco naumanni) suffered a sharp population decline over much of its European distribution range in the middle of the twentieth century. Still declining in some areas, the species has recently experienced a notable population recovery in certain regions. We examined the genetic diversity variation in a growing population of lesser kestrels from Central Spain over a 6-year period (2000–2005). The population studied showed a rapid demographic expansion, increasing in the number of both breeding pairs and colonies. Annual average heterozygosity and allelic diversity increased and genetic similarity between potential mates decreased over the study period. Several immigrants regularly arrived in the study area and introduced new alleles into the local population, pointing to immigration as the main cause contributing to the observed genetic recovery.