Aim We examined dorsal coloration in and genetic relationships among Iberian populations of the lizard Psammodromus algirus to determine the extent to which the current distribution of phenotypic variation is correlated with phylogeographical history or local environmental conditions. Location Iberian Peninsula, western Palaearctic. MethodsWe sequenced mitochondrial DNA (ND4 and adjacent tRNAs genes) in 36 populations, and seven microsatellite loci in eight representative populations. In 23 populations, lizards were classified according to the presence and intensity of a dorsal striped pattern, the heritability of which was estimated by means of mother-offspring regressions. To determine whether colour pattern is an adaptation for crypsis, we compared the time taken by humans to detect striped and unstriped lizards in different environments.Results The analysis of mtDNA revealed an ancient split between a western clade, subdivided into south-and north-western haplogroups, and an eastern clade with central, south-eastern and eastern haplogroups. In contrast, nuclear markers showed a post-glacial admixture of central and western haplogroups, with the central haplogroup apparently isolated from the rest of its clade. This was consistent with variation in the dorsal striped pattern, a heritable phenotypic trait: central and western lizards were unstriped, whereas eastern lizards were striped. We then suggest that dorsal coloration promotes crypsis: in eastern locations detection times were longer for striped than for unstriped lizards, whereas the opposite was true in western and central locations. Main conclusionsOur results indicate that natural selection for crypsis may promote not only divergence within clades, as suggested by the apparent isolation between unstriped central lizards and striped members of eastern haplogroups, but also admixture between them. We conclude that ecologically driven selection is crucial for understanding the phylogeographical background of phenotypic variation, because recent adaptation to the environment can blur the effects of ancestral isolation.
In the context of the immunocompetence handicap hypothesis, we explored how differences in parasite load affect the way in which sexual ornaments codify information about individual quality. We studied variation in sexual signals in two Iberian populations of the lizard Psammodromus algirus, a species in which sexually active males display a red head coloration. In one population, males were free of tick nymphs, whereas in the other one all males were tick-infested (mean of 12.7 tick nymphs/individual).At the onset of the breeding season, the red-coloured surface was larger in the non-parasitized population than in the parasitized one, whereas the opposite was true for colour saturation. We experimentally simulated a bacterial infection (by intraperitoneal injection of lipopolysaccharide) to examine the effects of immune activation on the expression of this sexual ornament. In the non-parasitized population, our treatment caused a reduction in the red-coloured surface of experimental males, whereas in the parasitized population it caused a decrease in colour saturation. In the parasitized population, males that displayed sexual coloration were larger, and had fewer parasites, than uncoloured ones, and inflammatory response to lipopolysaccharide injection in the palm of the hind paw was negatively correlated with colour saturation, but not with colour extension. Thus, we suggest parasites not only constrained the expression of sexual ornaments, but they also changed the signal properties that conveyed useful information about the quality of their bearers.
Local adaptation is a dynamic process by which different allele combinations are selected in different populations at different times, and whose genetic signature can be inferred by genome‐wide outlier analyses. We combined gene flow estimates with two methods of outlier detection, one of them independent of population coancestry (CIOA) and the other one not (ROA), to identify genetic variants favored when ecology promotes phenotypic convergence. We analyzed genotyping‐by‐sequencing data from five populations of a lizard distributed over an environmentally heterogeneous range that has been changing since the split of eastern and western lineages ca. 3 mya. Overall, western lizards inhabit forest habitat and are unstriped, whereas eastern ones inhabit shrublands and are striped. However, one population (Lerma) has unstriped phenotype despite its eastern ancestry. The analysis of 73,291 SNPs confirmed the east–west division and identified nonoverlapping sets of outliers (12 identified by ROA and 9 by CIOA). ROA revealed ancestral adaptive variation in the uncovered outliers that were subject to divergent selection and differently fixed for eastern and western populations at the extremes of the environmental gradient. Interestingly, such variation was maintained in Lerma, where we found high levels of heterozygosity for ROA outliers, whereas CIOA uncovered innovative variants that were selected only there. Overall, it seems that both the maintenance of ancestral variation and asymmetric migration have counterbalanced adaptive lineage splitting in our model species. This scenario, which is likely promoted by a changing and heterogeneous environment, could hamper ecological speciation of locally adapted populations despite strong genetic structure between lineages.
Our understanding about viruses carried by wild animals is still scarce. The viral diversity of wildlife may be best described with discovery-driven approaches to the study of viral diversity that broaden research efforts towards non-canonical hosts and remote geographic regions. Birds have been key organisms in the transmission of viruses causing important diseases, and wild birds are threatened by viral spillovers associated with human activities. However, our knowledge of the avian virome may be biased towards poultry and highly pathogenic diseases. We describe and compare the fecal virome of two passerine-dominated bird assemblages sampled in a remote Neotropical rainforest in French Guiana (Nouragues Natural Reserve) and a Mediterranean forest in central Spain (La Herrería). We used metagenomic data to quantify the degree of functional and genetic novelty of viruses recovered by examining if the similarity of the contigs we obtained to reference sequences differed between both locations. In general, contigs from Nouragues were significantly less similar to viruses in databases than contigs from La Herrería using Blastn but not for Blastx, suggesting that pristine regions harbor a yet unknown viral diversity with genetically more singular viruses than more studied areas. Additionally, we describe putative novel viruses of the families Picornaviridae, Reoviridae and Hepeviridae. These results highlight the importance of wild animals and remote regions as sources of novel viruses that substantially broaden the current knowledge of the global diversity of viruses.
There is a general and solid theoretical framework to explain how the interplay between natural selection and gene flow affects local adaptation. Yet, to what extent coexisting closely related species evolve collectively or show distinctive evolutionary responses remains a fundamental question. To address this, we studied the population genetic structure and morphological differentiation of sympatric three-spined and nine-spined stickleback. We conducted genotyping-by-sequencing and morphological trait characterisation using 24 individuals of each species from four lowland brackish water (LBW), four lowland freshwater (LFW) and three upland freshwater (UFW) sites in Belgium and the Netherlands. This combination of sites allowed us to contrast populations from isolated but environmentally similar locations (LFW vs. UFW), isolated but environmentally heterogeneous locations (LBW vs. UFW), and well-connected but environmentally heterogenous locations (LBW vs. LFW). Overall, both species showed comparable levels of genetic diversity and neutral genetic differentiation. However, for all three spatial scales, signatures of morphological and genomic adaptive divergence were substantially stronger among populations of the three-spined stickleback than among populations of the nine-spined stickleback. Furthermore, most outlier SNPs in the two species were associated with local freshwater sites. The few outlier SNPs that were associated with the split between brackish water and freshwater populations were located on one linkage group in three-spined stickleback and two linkage groups in nine-spined stickleback. We conclude that while both species show congruent evolutionary and genomic patterns of divergent selection, both species differ in the magnitude of their response to selection regardless of the geographical and environmental context.
During geographical expansion of a species individual colonizers have to confront different ecological challenges, and the capacity of the species to broaden its range may depend on the total amount of adaptive genetic variation supplied by evolution. We set out to test whether the distribution of loci under selection along a contrasting environmental gradient can be turned into a model that accurately predicts a species’ range. If positive, this may shed light on the genetic source of adaptive limits that shape range boundaries. We sampled five populations of the western Mediterranean lizard Psammodromus algirus that inhabit a noticeable environmental gradient of temperature and precipitation. We used 21 SNPs putatively under selection to correlate the genotypes of 95 individuals with environmental variation among their populations, using 1x1 km2 grid cells as sampling units. By extrapolating the resulting model to all possible combinations of alleles, we inferred the locations that were theoretically suitable for the species. The inferred distribution range overlapped to a large extent with the realized range of the species, including an accurate prediction of internal gaps and range borders. Our results suggest an adaptability threshold determined by the amount of genetic variation available that would be required to warrant adaptation beyond a certain limit of environmental variation. These results support the idea that the expansion of a species’ range may be ultimately linked to the arising of new variants under selection.
During the historical building of a species range, individual colonizers have to confront different ecological challenges, and the capacity of the species to broaden its range may depend on the total amount of adaptive genetic variation supplied by evolution.We set out to increase our understanding of what defines a range and the role of underlying genetics by trying to predict an entire species' range from the geographical distribution of its genetic diversity under selection. We sampled five populations of the western Mediterranean lizard Psammodromus algirus that inhabit a noticeable environmental gradient of temperature and precipitation. We correlated the genotypes of 95 individuals (18-20 individuals per population) for 21 SNPs putatively under selection with environmental scores on a bioclimatic gradient, using 1 × 1 km 2 grid cells as sampling units. By extrapolating the resulting model to all possible combinations of alleles, we inferred all the geographic cells that were theoretically suitable for a given amount of genetic variance under selection. The inferred distribution range overlapped to a large extent with the realized range of the species (77.46% of overlap), including an accurate prediction of internal gaps and range borders. Our results suggest an adaptability threshold determined by the amount of genetic variation available that would be required to warrant adaptation beyond a certain limit of environmental variation. These results support the idea that the expansion of a species' range can be ultimately linked to the arising of new variants under selection (either newly selected variants from standing genetic variation or innovative mutations under selection). K E Y W O R D Slocal adaptation, landscape genetics, range boundaries, reptilesarbitrary boundaries to range expansion, Haldane (1956) proposed gene "swamping" as a centre-border effect by which gene flow from central to marginal habitats causes maladaptation at the edges of the range, reducing population density and constraining range expansion. This dynamic pattern would jeopardize adaptation at the edge of the range, even if the genetic variants that could promote range expansion are present in the genetic pool of a species, because gene swamping would hamper a rise in the frequencies of adaptive alleles at range limits (Haldane, 1956). However, this hypothesis has been subject to continuous debate (Nosil & Crespi, 2004;Polechová, 2018;Sexton et al., 2011). Another possibility is that range limits arise because a species has fully colonized the spatial projection of its ecological niche, in such way that niche expansion must precede range enlargement (Hutchinson, 1957). In such cases, since niche
Isolation owing to anthropogenic habitat fragmentation is expected to increase the homozygosity of individuals, which might reduce their fitness as a result of inbreeding depression. Using samples from a fragmented population of the lizard Psammodromus algirus, for which we had data about two correlates of fitness, we genotyped individuals for six microsatellite loci that correctly capture genome-wide individual homozygosity of these lizards (as validated with an independent sample of lizards genotyped for both these microsatellites and > 70 000 single nucleotide polymorphisms). Our data revealed genetic structure at a very small geographical scale, which was compatible with restricted gene flow among populations disconnected in a matrix of inhospitable habitat. Lizards from the same fragment were genetically more related to one another than expected by chance, and individual homozygosity was greater in small than in large fragments. Within fragments, individual homozygosity was negatively associated with adult body size and clutch mass, revealing a link among reduced gene flow, increased homozygosity and lowered fitness that might reduce population viability deterministically. Our results contribute to mounting evidence of the impact of the loss of genetic diversity on fragmented wild populations.
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