Pedro J. Cordero

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.

Effects of paternal care on reproductive success in the polygynous spotless starling Sturnus unicolor

Abstract For males of socially polygynous avian species like the spotless starling, there may exist a trade-off between investing in paternal care and controlling several nests. To determine how the intensity of paternal care affects reproductive success per brood sired or expressed as the total number of young raised in all nests controlled by the same male, it is necessary to manipulate paternal care. Testosterone (T) has been shown to depress the tendency for males to care for their young, and induces them to acquire more mates. The effects of paternal care on reproductive success were studied by treating certain male starlings with exogenous T and others with the antiandrogen cyproterone acetate (CA), and comparing the parental behavior of T- and CA-males throughout the breeding season with that of controls. CA-males fed their chicks more during the first week after hatching than T-males, with controls feeding at intermediate rates, both on a per nest basis and as total effort for all nests controlled by the same male. Paternal feeding rates during the first week of chick life had a significant positive effect on the number of fledged young. The hormone treatment significantly affected the number of chicks raised per nest, CA-males having a higher breeding success per nest than T-males, and controls showing intermediate levels of success. There was no significant effect of treatment on total reproductive success attained by males throughout the season. In the polygonous spotless starling, the intensity of paternal care of young affects reproductive success per nest positively but not on a seasonal basis.

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.

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.

Within-clutch patterns of egg viability and paternity in the House Sparrow

One of the potential benefits of extra-pair copulation is an enhanced likelihood of successful fertilization if the pair male is unable to produce sufficient viable sperm to ensure the fertility of an entire clutch. Low male fertility can be a transient phenomenon associated with higher rates of sperm usage than production, leading to a progressive depletion of sperm reserves. Evidence of a correlation between hatching success and the occurrence of extra-pair fertilizations has been reported in House Sparrows. In this study we have used single-locus minisatellite and microsatellite profiling to investigate the distribution of extra-pair fertilizations within House Sparrow broods to determine whether there are changes in the level of hatching failure or extra-pair paternity during the course of producing a clutch. Embryonic material was collected at mid-incubation to minimize loss of data through pre-sampling mortality and to ensure that laying order was known. A significant clustering of both infertile eggs and extra-pair young was noted in the earliest eggs in a clutch. Possible causes of this phenomenon are discussed.

Population genetics of Mioscirtus wagneri, a grasshopper showing a highly fragmented distribution

The genetic consequences of population fragmentation and isolation are major issues in conservation biology. In this study we analyse the genetic variability and structure of the Iberian populations of Mioscirtus wagneri, a specialized grasshopper exclusively inhabiting highly fragmented hypersaline low grounds. For this purpose we have used seven species‐specific microsatellite markers to type 478 individuals from 24 localities and obtain accurate estimates of their genetic variability. Genetic diversity was relatively low and we detected genetic signatures suggesting that certain populations of M. wagneri have probably passed through severe demographic bottlenecks. We have found that the populations of this grasshopper show a strong genetic structure even at small geographical scales, indicating that they mostly behave as isolated populations with low levels of gene flow among them. Thus, several populations can be regarded as independent and genetically differentiated units which require adequate conservation strategies to avoid eventual extinctions that in highly isolated localities are not likely to be compensated for with the arrival of immigrants from neighbouring populations. Overall, our results show that these populations probably represent the ‘fragments’ of a formerly more widespread population and highlight the importance of protecting Iberian hypersaline environments due to the high number of rare and endangered species they sustain.

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.