Mercedes Molina-Morales

High-utility conserved avian microsatellite markers enable parentage and population studies across a wide range of species

BackgroundMicrosatellites are widely used for many genetic studies. In contrast to single nucleotide polymorphism (SNP) and genotyping-by-sequencing methods, they are readily typed in samples of low DNA quality/concentration (e.g. museum/non-invasive samples), and enable the quick, cheap identification of species, hybrids, clones and ploidy. Microsatellites also have the highest cross-species utility of all types of markers used for genotyping, but, despite this, when isolated from a single species, only a relatively small proportion will be of utility. Marker development of any type requires skill and time. The availability of sufficient “off-the-shelf” markers that are suitable for genotyping a wide range of species would not only save resources but also uniquely enable new comparisons of diversity among taxa at the same set of loci. No other marker types are capable of enabling this. We therefore developed a set of avian microsatellite markers with enhanced cross-species utility.ResultsWe selected highly-conserved sequences with a high number of repeat units in both of two genetically distant species. Twenty-four primer sets were designed from homologous sequences that possessed at least eight repeat units in both the zebra finch (Taeniopygia guttata) and chicken (Gallus gallus). Each primer sequence was a complete match to zebra finch and, after accounting for degenerate bases, at least 86% similar to chicken. We assessed primer-set utility by genotyping individuals belonging to eight passerine and four non-passerine species. The majority of the new Conserved Avian Microsatellite (CAM) markers amplified in all 12 species tested (on average, 94% in passerines and 95% in non-passerines). This new marker set is of especially high utility in passerines, with a mean 68% of loci polymorphic per species, compared with 42% in non-passerine species.ConclusionsWhen combined with previously described conserved loci, this new set of conserved markers will not only reduce the necessity and expense of microsatellite isolation for a wide range of genetic studies, including avian parentage and population analyses, but will also now enable comparisons of genetic diversity among different species (and populations) at the same set of loci, with no or reduced bias. Finally, the approach used here can be applied to other taxa in which appropriate genome sequences are available.

Assessing the effects of climate on host-parasite interactions: a comparative study of European birds and their parasites.

Background Climate change potentially has important effects on distribution, abundance, transmission and virulence of parasites in wild populations of animals. Methodology/Principal Finding Here we analyzed paired information on 89 parasite populations for 24 species of bird hosts some years ago and again in 2010 with an average interval of 10 years. The parasite taxa included protozoa, feather parasites, diptera, ticks, mites and fleas. We investigated whether change in abundance and prevalence of parasites was related to change in body condition, reproduction and population size of hosts. We conducted analyses based on the entire dataset, but also on a restricted dataset with intervals between study years being 5–15 years. Parasite abundance increased over time when restricting the analyses to datasets with an interval of 5–15 years, with no significant effect of changes in temperature at the time of breeding among study sites. Changes in host body condition and clutch size were related to change in temperature between first and second study year. In addition, changes in clutch size, brood size and body condition of hosts were correlated with change in abundance of parasites. Finally, changes in population size of hosts were not significantly related to changes in abundance of parasites or their prevalence. Conclusions/Significance Climate change is associated with a general increase in parasite abundance. Variation in laying date depended on locality and was associated with latitude while body condition of hosts was associated with a change in temperature. Because clutch size, brood size and body condition were associated with change in parasitism, these results suggest that parasites, perhaps mediated through the indirect effects of temperature, may affect fecundity and condition of their hosts. The conclusions were particularly in accordance with predictions when the restricted dataset with intervals of 5–15 years was used, suggesting that short intervals may bias findings.

Factors affecting natal and breeding magpie dispersal in a population parasitized by the great spotted cuckoo

Understanding the causes and consequences of avian dispersal is important since dispersal movements may influence individuals’ survival and reproductive success. Although obligate interspecific brood parasitism has obvious detrimental effects for its avian host, few empirical studies have addressed the question of how brood parasitism may influence host dispersal. We studied factors affecting, and consequences of, natal and breeding dispersal movements in a population of magpies, Pica pica, parasitized by the great spotted cuckoo, Clamator glandarius, by monitoring dispersal of individuals and cuckoo parasitism over 6 years. Recruitment probability increased with fledging weight and was higher for individuals hatching early in the breeding season. Heaviest recruits at fledging settled closer to their natal nests and bred in more saturated sites within the study area. Natal dispersal distance did not predict the magpie’s productivity or risk of cuckoo parasitism in its first reproductive attempt. Females and parasitized males decreased their breeding dispersal distance when breeding close to other pairs, whereas nonparasitized males breeding close to other pairs dispersed more in subsequent years. Females, but not males, breeding closer to their previous breeding places had larger clutches than those breeding further away. Dispersing longer or shorter distances between breeding attempts had no consequences in terms of cuckoo parasitism avoidance for magpies. Our results suggest a minor role of great spotted cuckoo parasitism on magpie dispersal movements at the spatial scale analysed. Instead, our study revealed density-dependent dispersal in our parasitized magpie population.

Evidence of long‐term structured cuckoo parasitism on individual magpie hosts

Brood parasites usually reduce their hosts breeding success, resulting in strong selection for the evolution of host defences. Intriguingly, some host individuals/populations show no defence against parasitism, which has been explained within the frame of three different evolutionary hypotheses. One of these hypotheses posits that intermediate levels of defence at the population level may result from nonrandom distribution of parasitism among host individuals (i.e. structured parasitism). Empirical evidence for structured brood parasitism is, however, lacking for hosts of European cuckoos due to the absence of long-term studies. Here, we seek to identify the patterns of structured parasitism by studying great spotted cuckoo parasitism on individual magpie hosts over five breeding seasons. We also aim to identify whether individual characteristics of female magpies and/or their territories were related to the status of repeated parasitism. We found that 28·3% of the females in our population consistently escaped from cuckoo parasitism. Only 11·3% of females were always parasitized, and the remaining 60·4% changed their parasitism status. The percentage of females that maintained their status of parasitism (i.e. either parasitized or nonparasitized) between consecutive years varied over the study. Females that never suffered cuckoo parasitism built bigger nests than parasitized females at the beginning of the breeding season and smaller nests than those of parasitized females later in the season. Nonparasitized females also moved little from year to year and preferred areas with different characteristics over the course of the breeding season than parasitized females. Overall, females escaping from cuckoo parasitism reared twice as many chicks per year than those that were parasitized. In conclusion, our study reveals for first time the existence of a structured pattern of cuckoo parasitism based on phenotypic characteristics of individual hosts and of their territories.

CUCKOO HOSTS SHIFT FROM ACCEPTING TO REJECTING PARASITIC EGGS ACROSS THEIR LIFETIME

One of the best‐known outcomes of coevolution between species is the rejection of mimetic parasite eggs by avian hosts, which has evolved to reduce costly cuckoo parasitism. How this behavioral adaptation varies along the life of individual hosts remains poorly understood. Here, we identify for the first time, lifetime patterns of egg rejection in a parasitized long‐lived bird, the magpie Pica pica and show that, during the years they were studied, some females accept, others reject, and some others modify their response to model eggs, in all cases switching from acceptance to rejection. Females tested in their first breeding attempt always accepted the model egg, even those individuals whose mothers were egg rejecters. A longitudinal analysis showed that the probability of egg rejection increased with the relative age of the female, but was not related to the risk of parasitism in the population. We conclude that ontogeny plays a fundamental role in the process leading to egg rejection in magpies.

The multidimensionality of behavioural defences against brood parasites: evidence for a behavioural syndrome in magpies?

Studies of antiparasite defences against cuckoo parasites have largely neglected the possibility that behavioural components of host defence may correlate giving rise to a behavioural syndrome. Furthermore, the different contribution of the host’s sex in nest defence has traditionally been disregarded. Here, we studied magpie (Pica pica) mobbing behaviour towards dummies of great spotted cuckoo (Clamator glandarius) and non-harmful hoopoes (Upupa epops) and egg rejection of parasite eggs in a population of colour-banded magpies. We predicted a positive correlation between the intensity of nest defence and egg rejection within each sex and that females respond more intensely than males to the threat of brood parasitism as they undertake incubation. Magpie males, but not females, defended their nests more intensely in those nests in which cuckoo model eggs were rejected. Individual magpies did significantly differ in their baseline level of nest attentiveness; however, there were no individual differences once pair identity was considered. Males and females defended their nests more intensely when it was exposed to the presence of a great spotted cuckoo dummy. Males, but not females, were more prone to appear at their nests, and females, but not males, were more prone to defend more intensely when their nests were challenged by a parasite threat. Our results thus agree with the view that mobbing behaviour and egg rejection in magpies may actually constitute a pseudosyndrome and highlight the necessity to integrate interindividual variation and the sex of the host in studies of the evolution of host defences.

Do climatic conditions affect host and parasite phenotypes differentially? A case study of magpies and great spotted cuckoos

Climatic conditions, through their effects on resource availability, may affect important life history strategies and trade-offs in animals, as well as their interactions with other organisms such as parasites. This impact may depend on species-specific pathways of development that differ even among species with similar resource requirements (e.g., avian brood parasites and their hosts). Here we explore the degree of covariation between environmental-climatic conditions and nestling phenotypes (i.e., tarsus length, body mass, immune response to phytohemagglutinin injection) and ectoparasite loads of great spotted cuckoos (Clamator glandarius) and those of their magpie (Pica pica) hosts, both within and among 11 study years (1997–2011). Our main results were that (1) nestling phenotypes differed among years, but differently for great spotted cuckoos and magpies; (2) nestling phenotypes showed significant among-year covariation with breeding climatic conditions (temperature and precipitation); and (3) these associations differed for cuckoos and magpies for some phenotypic traits. As the average temperature at the beginning of the breeding season (April) increased, body mass and tarsus length increased only for cuckoos, but not for magpie hosts, while immune response decreased in both species. Finally, (4) the strength of the within-year relationships between the probability of ectoparasitism by Carnushemapterus flies and laying date (used as an estimate of the within-year variation in climatic conditions) was negatively affected by the annual accumulated precipitation in April. These results strongly suggest that variation in climatic conditions would result in asymmetric effects on different species with respect to the probability of ectoparasitism, immunity and body size. Such asymmetric effects may affect animal interactions in general and those of brood parasites and their hosts in particular.

Characterization of 28 microsatellite loci in the European roller Coracias garrulus (Coracidae, AVES)

One hundred and forty-four existing microsatellite avian loci were tested for polymorphism in two to four unrelated European rollers. This allowed the identification of 28 unique polymorphic loci that we characterized in 34 unrelated individuals from a population in Guadix, Spain. The putative chromosomal locations of all the polymorphic loci in European rollers could be assigned based on the location of their orthologues in the assembled zebra finch and chicken genomes. All loci were assigned to autosomes based on predictive mapping and/or the presence of female heterozygotes, except CAM-11 that was assigned to the Z chromosome. By using a selected subset of 15 autosomal loci, the combined non-exclusion probability for identity was 4.7E-09.

Host nest site choice depends on risk of cuckoo parasitism in magpie hosts

Avian brood parasites impose large fitness costs on their hosts and, thus, brood parasitism has selected for an array of host defensive mechanisms to avoid them. So far most studies have focused on antiparasite defenses operating at the egg and chick stages and neglected defenses that may work prior to parasite egg deposition. Here, we experimentally explore the possibility that hosts, as part of a front-line defense, might minimize parasitism costs through informed nest site choice based on perceived risk of cuckoo parasitism. We conducted a large-scale manipulation of visual and auditory cues potentially informing on the risk of great spotted cuckoo Clamator glandarius parasitism during the nest site choice period of the magpie Pica pica host to investigate its effect on host’s nest settlement and individual year to year site fidelity. Early breeding magpies preferentially placed their nests in safe areas (i.e., in sites of low perceived risk of parasitism), and, this effect diluted with time elapsed since risk of parasitism was manipulated. Site fidelity of individual magpies decreased with risk of cuckoo parasitism, for those that were not parasitized in the previous year. Our results constitute the first strong evidence showing that hosts can minimize the costs of cuckoo parasitism through informed nest-site choice, calling for future consideration of defenses potentially operating prior to parasite egg deposition to achieve a better understanding of cuckoo-host coevolution.

An experimental test of host’s life history traits modulation in response to cuckoo parasitism risk

Hosts can counteract parasites through defences based on resistance and/or tolerance. The mechanistic basis of tolerance, which involve defensive mechanisms minimizing parasite damage after a successful parasitic attack, remains poorly explored in the study of cuckoo-host interactions. Here, we experimentally explore the possibility that the risk of great spotted cuckoo Clamator glandarius parasitism may induce tolerance defences in magpie Pica pica hosts through plasticity in life-history traits. We predict that magpies exposed to auditory cues indicating high parasitism risk will more likely exhibit resistance and/or modify their life-history traits to minimize parasitism costs (i.e. tolerance) compared to magpies under low parasitism risk. We found that manipulating the perceived parasitism risk did not affect host resistance (i.e. rejection of parasitic eggs) nor host life-history traits. Unexpectedly, host’s egg volume increased over the season in nests exposed to auditory cues of control non-harmful hoopoes Upupa epops. Our results do not provide support for inducible defences (either based on resistance or tolerance) in response to risk of parasitism in magpie hosts. Even so, we encourage studying plastic expression of breeding strategies in response to risk of cuckoo parasitism to achieve a better understanding of the mechanistic basis of tolerance defences.