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Illera, J. C.

Publications and source records attributed to Illera, J. C..

7 recordsLinked to original sources

From migrants to residents: Genomic insights into adaptive strategies in European robins (Erithacus rubecula)

Bird migration evolved as an adaptation to seasonally changing habitats. Migratory behaviour can vary within the same species in case of partial migratory behaviour, i.e. one population (or individual) is migratory and another one is resident. Species that exhibit a wide variety of migratory phenotypes provide valuable systems to understand the evolutionary drivers behind different phenotypes and how populations adapt to habitats with distinct seasonality. The European robin (Erithacus rubecula) expresses migratory behaviour in central and northern areas of the species distribution range, whereas populations in the South and on the Macaronesian islands are predominantly resident, providing a suitable system to investigate these questions. We use high coverage whole genome re-sequencing data of 125 European robins to investigate how migration behaviour affects population structure and demography, and how it affects the selection landscape in the genome. Genetic structure in European robins coincides with migratory phenotype and geography and populations are characterised by distinct demographic histories. Our results suggest that both the continental resident population as well as the Macaronesian island populations have derived independently from an ancestral migratory population. Unexpectedly, tests for differential selection revealed extensive positive selection pressure acting across all chromosomes in the resident populations, while selective sweeps are largely absent from migrants. We speculate that this might be an analytical artifact due to mismatching timescales between what population genomics methods can detect and the scale on which migration behaviour likely evolved in the robin. We suggest that future studies on the genomics of migration should more focally account for different time scales on which these processes happen, such as including the wider phylogenomic background of the target species, to capture the full evolutionary history of migratory traits.

evolutionary biology↗

Host filtering and biogeography structure island bird gut microbiomes

Gut microbiomes are central to host ecology and evolution, yet the mechanisms driv-ing their diversification remain elusive, partly because host evolution and biogeography are often confounded. The recent radiation of chaffinches in Macaronesia, coupled with their broadly similar ecologies across islands, makes them an ideal replicated natural experiment to separate spatial from host-driven effects on microbiome structure. Us-ing long-read 16S rRNA gene sequencing, diet metabarcoding, and whole-genome host data, we show that gut microbiome diversity aligns with predictions of island biogeog-raphy theory rather than host colonization history, revealing that microbial dispersal limitation independent of the host is a dominant mechanism of community assembly. Geography and diet primarily explain bacterial presence-absence patterns, whereas host genetic differentiation and heterozygosity influence abundant, potentially resident taxa. Challenging previous assumptions about birds, we detect clear signals of phylosymbiosis (i.e. similar microbiome composition among closely related hosts), however phylogenetic reconciliation reveals these associations result from convergent host filtering of environ-mentally acquired bacteria, likely via shared diets or physiological traits, rather than de-tectable co-diversification. Our study reframes our understanding of avian host-microbe relationships, revealing that birds maintain host-specific microbiome associations within biogeographic constraints, but these arise from ecological filtering processes rather than co-evolutionary partnerships.

evolutionary biology↗

Population-specific association of Clock gene polymorphism with annual cycle timing in stonechats

Timing is essential for survival and reproduction of organisms across the tree of life. The core circadian clock gene Clk has been implicated in annual timing and shows highly conserved sequence homology across vertebrates except for one variable region of poly Glutamine repeats. Clk genotype varies in some species with latitude, seasonal timing and migration. However, findings are inconsistent, difficult to disentangle from environmental responses, and biased towards high latitudes. Here we combine field data with a common-garden set up to study associations of Clk with latitude, migration and annual-cycle timing within the stonechat species complex with trans-equatorial distribution range. Including 950 individuals from nine populations with diverse migratory strategies. Gene diversity was lowest in resident African and Canary Island populations and increased with latitude, independently of migration distance. Repeat length and annual-cycle timing was linked in a population-specific way. Specifically, equatorial African stonechats showed delayed timing with longer repeat length for all annual-cycle stages. Our data suggest that at low latitudes with constant photoperiod, Clk genotype might orchestrate a range of consistent, individual chronotypes. In contrast, the influence of Clk on annual-cycle timing at higher latitudes might be mediated by its interactions with genes involved in (circadian) photoperiodic pathways.

genetics↗

Recombination suppression and selection affect local ancestries in genomes of a migratory songbird

Genetic variation of the entire genome represents population structure, yet individual loci can show distinct patterns. Such deviations identified through genome scans have often been attributed to effects of selection instead of randomness. This interpretation assumes that long enough genomic intervals average out randomness in underlying genealogies, which represent local genetic ancestries. However, an alternative explanation to distinct patterns has not been fully addressed: too few genealogies to average out the effect of randomness. Specifically, distinct patterns of genetic variation may be due to reduced local recombination rate, which reduces the number of genealogies in a genomic window. Here, we associate distinct patterns of local genetic variation with reduced recombination rates in a songbird, the Eurasian blackcap (Sylvia atricapilla), using genome sequences and recombination maps. We find that distinct patterns of local genetic variation reflect haplotype structure at low-recombining regions either shared in most populations or found only in a few populations. At the former species-wide low-recombining regions, genetic variation depicts conspicuous haplotypes segregating in multiple populations. At the latter population-specific low-recombining regions, genetic variation represents variance among cryptic haplotypes within the low-recombining populations. With simulations, we confirm that these distinct patterns of haplotype structure evolve due to reduced recombination rate, on which the effects of selection can be overlaid. Our results highlight that distinct patterns of genetic variation can emerge through evolution of reduced local recombination rate. Recombination landscape as an evolvable trait therefore plays an important role determining the heterogeneous distribution of genetic variation along the genome.

evolutionary biology↗

Reduction in population size and not a shift in parasite community affect evolution of immune genes in island birds.

AO_SCPLOWBSTRACTC_SCPLOWShared ecological conditions encountered by species that colonize islands often lead to the evolution of convergent phenotypes, commonly referred to as "island syndrome". Reduced immune functions have been previously proposed to be part of this syndrome, as a consequence of the reduced diversity of pathogens on island ecosystems. According to this hypothesis, immune genes are expected to exhibit genomic signatures of relaxed selection pressure in island species. In this study, we used comparative genomic methods to study immune genes in island species (N = 20) and their mainland relatives (N = 14). We gathered public data as well as generated new data on innate (TLR: Toll-Like Receptors, BD: Beta Defensins) and acquired immune genes (MHC: Major Histocompatibility Complex classes I and II), but also on hundreds of genes with various immune functions. As a control, we used a set of 97 genes, not known to be involved in immune functions based on the literature, to account for the increased drift effects of the lower effective population sizes in island species. We used synonymous and non-synonymous variants to estimate the selection pressure acting on immune genes. We found that BDs and TLRs have higher ratios of non-synonymous over synonymous polymorphisms (Pn/Ps) than randomly selected control genes, suggesting that they evolve under a different selection regime. However, simulations show that this is unlikely to be explained by ongoing positive selection or balancing selection. For the MHC genes, which evolve under balancing selection, we used simulations to estimate the impact of population size variation. We found a significant effect of drift on immune genes of island species leading to a reduction in genetic diversity and efficacy of selection. However, the intensity of relaxed selection was not significantly different from control genes, except for MHC class II genes. These genes exhibit a significantly higher level of non-synonymous loss of polymorphism than expected assuming only drift and evolution under frequency dependent selection, possibly due to a reduction of extracellular parasite communities on islands. Overall, our results showed that demographic effects lead to a decrease in the immune functions of island species, but the relaxed selection that is expected to be caused by a reduced parasite pressure may only occur in some categories of immune genes.

evolutionary biology↗

Endemic island songbirds as windows into evolution in small effective population sizes

Due to their limited ranges and inherent isolation, island species have long been recognized as crucial systems for tackling a range of evolutionary questions, including in the early study of speciation [1,2]. Such species have been less studied in the understanding of the evolutionary forces driving DNA sequence evolution. Island species usually have lower census population sizes (N) than continental species and, supposedly, lower effective population sizes (Ne). Given that both the rates of change caused by genetic drift and by selection are dependent upon Ne, island species are theoretically expected to exhibit (i) lower genetic diversity, (ii) less effective natural selection against slightly deleterious mutations [3,4], and (iii) a lower rate of adaptive evolution [5-8, see also Note S1]. Here, we have used a large set of newly sequenced and published whole genome sequences of Passerida bird species or subspecies (14 insular and 11 continental) to test these predictions. We empirically confirm that island species exhibit lower census size and Ne, supporting the hypothesis that the smaller area available on islands constrains the upper bound of Ne. In the insular species, we find significantly lower nucleotide diversity in coding regions, higher ratios of non-synonymous to synonymous polymorphisms, and lower adaptive substitution rates. Our results provide robust evidence that the lower Ne experienced by island species has affected both the ability of natural selection to efficiently remove weakly deleterious mutations and also the adaptive potential of island species, therefore providing considerable empirical support for the nearly neutral theory. We discuss the implications for both evolutionary and conservation biology.

evolutionary biology↗

Correlated patterns of genetic diversity and differentiation across an avian family

Comparative studies of genomic differentiation among independent lineages can provide insights into aspects of the speciation process, such as the relative importance of selection and drift in shaping genomic landscapes, the role of genomic regions of high differentiation, and the prevalence of convergent molecular evolution. We investigated patterns of genetic diversity and divergence in stonechats (genus Saxicola), a widely distributed avian species complex with phenotypic variation in plumage, morphology, and migratory behavior, to ask whether similar genomic regions are important in the evolution of independent, but closely related, taxa. We used whole-genome pooled sequencing of 262 individuals from 5 taxa and found that patterns of genetic diversity and divergence are highly similar among different stonechat taxa. We then asked if these patterns remain correlated at deeper evolutionary scales and found that homologous genomic regions have become differentiated in stonechats and the closely related Ficedula flycatchers. Such correlation across a range of evolutionary divergence and among phylogenetically independent comparisons suggests that similar processes may be driving the differentiation of these independently evolving lineages, which in turn may be the result of intrinsic properties of particular genomic regions (e.g., areas of low recombination). Consequently, studies employing genome scans to search for areas important in reproductive isolation should account for corresponding regions of differentiation, as these regions may not necessarily represent speciation islands or facilitate local adaptation.

genomics↗