Aileen Adam

Parental prey selection affects risk-taking behaviour and spatial learning in avian offspring

Early nutrition shapes life history. Parents should, therefore, provide a diet that will optimize the nutrient intake of their offspring. In a number of passerines, there is an often observed, but unexplained, peak in spider provisioning during chick development. We show that the proportion of spiders in the diet of nestling blue tits, Cyanistes caeruleus, varies significantly with the age of chicks but is unrelated to the timing of breeding or spider availability. Moreover, this parental prey selection supplies nestlings with high levels of taurine particularly at younger ages. This amino acid is known to be both vital and limiting for mammalian development and consequently found in high concentrations in placenta and milk. Based on the known roles of taurine in mammalian brain development and function, we then asked whether by supplying taurine-rich spiders, avian parents influence the stress responsiveness and cognitive function of their offspring. To test this, we provided wild blue tit nestlings with either a taurine supplement or control treatment once daily from the ages of 2–14 days. Then pairs of size- and sex-matched siblings were brought into captivity for behavioural testing. We found that juveniles that had received additional taurine as neonates took significantly greater risks when investigating novel objects than controls. Taurine birds were also more successful at a spatial learning task than controls. Additionally, those individuals that succeeded at a spatial learning task had shown intermediate levels of risk taking. Non-learners were generally very risk-averse controls. Early diet therefore has downstream impacts on behavioural characteristics that could affect fitness via foraging and competitive performance. Fine-scale prey selection is a mechanism by which parents can manipulate the behavioural phenotype of offspring.

Patterns of genetic diversity in outcrossing and selfing populations of Arabidopsis lyrata

Arabidopsis lyrata is normally considered an obligately outcrossing species with a strong self‐incompatibility system, but a shift in mating system towards inbreeding has been found in some North American populations (subspecies A. lyrata ssp. lyrata). This study provides a survey of the Great Lakes region of Canada to determine the extent of this mating system variation and how outcrossing rates are related to current population density, geographical distribution, and genetic diversity. Based on variation at microsatellite markers (progeny arrays to estimate multilocus outcrossing rates and population samples to estimate diversity measures) and controlled greenhouse pollinations, populations can be divided into two groups: (i) group A, consisting of individuals capable of setting selfed seed (including autogamous fruit set in the absence of pollinators), showing depressed outcrossing rates (Tm = 0.2–0.6), heterozygosity (HO = 0.02–0.06) and genetic diversity (HE = 0.08–0.10); and (ii) group B, consisting of individuals that are predominantly self‐incompatible (Tm > 0.8), require pollinators for seeds set, and showing higher levels of heterozygosity (HO = 0.13–0.31) and diversity (HE = 0.19–0.410). Current population density is not related to the shift in mating system but does vary with latitude. Restricted gene flow among populations was evident among all but two populations (FST = 0.11–0.8). Group A populations were more differentiated from one another (FST = 0.78) than they were from group B populations (FST = 0.59), with 41% of the variation partitioned within populations, 47% between populations, and 12% between groups. No significant relationship was found between genetic and geographical distance. Results are discussed in the context of possible postglacial expansion scenarios in relation to loss of self‐incompatibility.

Stress exposure in early post-natal life reduces telomere length: an experimental demonstration in a long-lived seabird

Exposure to stressors early in life is associated with faster ageing and reduced longevity. One important mechanism that could underlie these late life effects is increased telomere loss. Telomere length in early post-natal life is an important predictor of subsequent lifespan, but the factors underpinning its variability are poorly understood. Recent human studies have linked stress exposure to increased telomere loss. These studies have of necessity been non-experimental and are consequently subjected to several confounding factors; also, being based on leucocyte populations, where cell composition is variable and some telomere restoration can occur, the extent to which these effects extend beyond the immune system has been questioned. In this study, we experimentally manipulated stress exposure early in post-natal life in nestling European shags (Phalacrocorax aristotelis) in the wild and examined the effect on telomere length in erythrocytes. Our results show that greater stress exposure during early post-natal life increases telomere loss at this life-history stage, and that such an effect is not confined to immune cells. The delayed effects of increased telomere attrition in early life could therefore give rise to a ‘time bomb’ that reduces longevity in the absence of any obvious phenotypic consequences early in life.

From cradle to early grave: juvenile mortality in European shags Phalacrocorax aristotelis results from inadequate development of foraging proficiency

In most long-lived animal species, juveniles survive less well than adults. A potential mechanism is inferior foraging skills but longitudinal studies that follow the development of juvenile foraging are needed to test this. We used miniaturized activity loggers to record daily foraging times of juvenile and adult European shags Phalacrocorax aristotelis from fledging to the following spring. Juveniles became independent from their parents 40 days post-fledging. They compensated for poor foraging proficiency by foraging for approximately 3 h d−1 longer than adults until constrained by day length in early November. Thereafter, juvenile foraging time tracked shortening day length up to the winter solstice, when foraging time of the two age classes converged and continued to track day length until early February. Few individuals died until midwinter and mortality peaked in January–February, with juvenile mortality (including some of the study birds) five times that of adults. In their last two weeks of life, juveniles showed a marked decline in foraging time consistent with individuals becoming moribund. Our results provide compelling evidence that juveniles compensate for poor foraging proficiency by increasing foraging time, a strategy that is limited by day length resulting in high winter mortality.

Subtle manipulation of egg sex ratio in birds.

Mothers are predicted to overproduce male or female eggs when the relative fitness gains from one sex are higher and outweigh the costs of manipulation. However, in birds such biases are often difficult to distinguish from differential embryo or chick mortality. Using a molecular technique to identify the sex of early embryos, we aim to determine the effect of maternal nutrition on zebra finch (Taeniopygia guttata) egg sex ratios after 2 days of incubation, which is as close to conception as is currently possible. We found no overall bias in the sex ratio of eggs laid and sex did not differ with relative laying order under any diet regime. However, mothers on a low-quality diet did produce a female bias in small clutches and a slight male bias in large clutches. On a high-quality diet, mothers produced a male bias in small clutches and a female bias in large clutches. Those on a standard diet produced a roughly even sex ratio, irrespective of clutch size. These observed biases in egg sex are partly in line with predictions that, in this species, daughters suffer disproportionately from poor rearing conditions. Thus, when relatively malnourished, mothers should only rear daughters in small broods and vice versa. Sex-ratio patterns in this species therefore appear to be subtle.

Validation of swabs as a non-destructive and relatively non-invasive DNA sampling method in fish

Non‐destructive methods of collecting DNA from small fish species can be problematic, as fin clips can potentially affect behaviour or survivorship in the wild. Swabbing body mucus may provide a less invasive method of DNA collection. However, risk of contamination from other individuals in high density groups could give erroneous genotyping results. We compared multilocus microsatellite genotypes from the same individuals when collected at low and high density and compared this with fin clips. We found no differences between these categories, with a genotyping error rate of 0.42%, validating the use of body mucus swabbing for DNA collection in fish.

EFFECTS OF INCUBATION CONDITIONS AND OFFSPRING SEX ON EMBRYONIC DEVELOPMENT AND SURVIVAL IN THE ZEBRA FINCH (TAENIOPYGIA GUTTATA)

Abstract Suboptimal conditions during embryonic development can affect offspring fitness. Both egg quality and incubation behavior can affect hatching success, hatching mass, and subsequent offspring performance. These effects may differ between male and female offspring. We manipulated the prebreeding body condition of Zebra Finches (Taeniopygia guttata), using diets of different protein content. To separate possible effects on egg quality of parental body condition and incubation conditions, we did a cross-fostering experiment. We analyzed embryo survival and hatching mass with respect to body condition of the egg-laying parent, body condition of the incubating foster parent, and offspring sex. Embryos were not affected by the condition of the egg-laying parent. Eggs incubated by parents in better condition suffered less embryo mortality than those incubated by parents in poorer condition, but only when overall embryo mortality was low. Hatching mass was also affected by the incubating foster parent’s body condition. And hatchlings incubated by parents in good condition were heavier than those incubated by parents in poor condition. Female hatchlings from late-laid eggs were heavier, in comparison with the size of the egg from which they hatched, than female hatchlings from earlier-laid eggs. No such effect was found for males. Therefore, male and female embryos may differ in their sensitivity to suboptimal conditions during embryonic development. These results suggest that parental body condition during incubation can affect offspring fitness. Efectos de las Condiciones de Incubación y el Sexo de las Crías sobre el Desarrollo Embrional y la Supervivencia en Taeniopygia guttata

Absence of three known benzimidazole resistance mutations in Trichostrongylus tenuis, a nematode parasite of avian hosts

Benzimidazole (BZ) resistance is widespread in nematode parasites of livestock, but very little is known about the levels of BZ resistance in parasites with avian hosts. We investigated BZ resistance in Trichostrongylus tenuis, a nematode parasite of red grouse, Lagopus lagopus scotica. BZ anthelmintics had been in use in this system for up to 15 years, yet existing phenotypic evidence for resistance was inconclusive. We screened 1530 individuals from 14 populations at the principal beta-tubulin locus for BZ resistance (isotype 1, residue 200) and 940 of these at two further resistance sites (isotype 1, residue 167; isotype 2, residue 200). No BZ resistant genotypes were found. Alternative mechanisms may be responsible for BZ resistance in this system, or the method and timing of treatments may reduce selection pressure for BZ resistance by creating substantial refugia for susceptible genotypes.

What causes mating system shifts in plants? Arabidopsis lyrata as a case study

The genetic breakdown of self-incompatibility (SI) and subsequent mating system shifts to inbreeding has intrigued evolutionary geneticists for decades. Most of our knowledge is derived from interspecific comparisons between inbreeding species and their outcrossing relatives, where inferences may be confounded by secondary mutations that arose after the initial loss of SI. Here, we study an intraspecific breakdown of SI and its consequences in North American Arabidopsis lyrata to test whether: (1) particular S-locus haplotypes are associated with the loss of SI and/or the shift to inbreeding; (2) a population bottleneck may have played a role in driving the transition to inbreeding; and (3) the mutation(s) underlying the loss of SI are likely to have occurred at the S-locus. Combining multiple approaches for genotyping, we found that outcrossing populations on average harbour 5 to 9 S-locus receptor kinase (SRK) alleles, but only two, S1 and S19, are shared by most inbreeding populations. Self-compatibility (SC) behaved genetically as a recessive trait, as expected from a loss-of-function mutation. Bulked segregant analysis in SC × SI F2 individuals using deep sequencing confirmed that all SC plants were S1 homozygotes but not all S1 homozygotes were SC. This was also revealed in population surveys, where only a few S1 homozygotes were SC. Together with crossing data, this suggests that there is a recessive factor that causes SC that is physically unlinked to the S-locus. Overall, our results emphasise the value of combining classical genetics with advanced sequencing approaches to resolve long outstanding questions in evolutionary biology.

Inbreeding depression in self-incompatible North-American Arabidopsis lyrata: disentangling genomic and S-locus-specific genetic load

Newly formed selfing lineages may express recessive genetic load and suffer inbreeding depression. This can have a genome-wide genetic basis, or be due to loci linked to genes under balancing selection. Understanding the genetic architecture of inbreeding depression is important in the context of the maintenance of self-incompatibility and understanding the evolutionary dynamics of S-alleles. We addressed this using North-American subspecies of Arabidopsis lyrata. This species is normally self-incompatible and outcrossing, but some populations have undergone a transition to selfing. The goals of this study were to: (1) quantify the strength of inbreeding depression in North-American populations of A. lyrata; and (2) disentangle the relative contribution of S-linked genetic load compared with overall inbreeding depression. We enforced selfing in self-incompatible plants with known S-locus genotype by treatment with CO2, and compared the performance of selfed vs outcrossed progeny. We found significant inbreeding depression for germination rate (δ=0.33), survival rate to 4 weeks (δ=0.45) and early growth (δ=0.07), but not for flowering rate. For two out of four S-alleles in our design, we detected significant S-linked load reflected by an under-representation of S-locus homozygotes in selfed progeny. The presence or absence of S-linked load could not be explained by the dominance level of S-alleles. Instead, the random nature of the mutation process may explain differences in the recessive deleterious load among lineages.