Hybridization facilitates recombination between divergent genetic lineages and can be shaped by both neutral and selective processes. Upon hybridization, loci with no net fitness effects introgress randomly from parental species into the genomes of hybrid individuals. Conversely, alleles from one parental species at some loci may provide a selective advantage to hybrids, resulting in patterns of introgression that do not conform to random expectations. We investigated genomic patterns of differential introgression in natural hybrids of two species of Caribbean anoles,
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Abstract Anolis pulchellus andA. krugi in Puerto Rico. Hybrids exhibitA. pulchellus phenotypes but possessA. krugi mitochondrial DNA, originated from multiple, independent hybridization events, and appear to have replaced pureA. pulchellus across a large area in western Puerto Rico. Combining genome‐wide SNP datasets with bioinformatic methods to identify signals of differential introgression in hybrids, we demonstrate that the genomes of hybrids are dominated bypulchellus ‐derived alleles and show only 10%–20%A. krugi ancestry. The majority ofA. krugi loci in hybrids exhibit a signal of non‐random differential introgression and include loci linked to genes involved in development and immune function. Three of these genes (delta like canonical notch ligand 1, jagged1 and notch receptor 1) affect cell differentiation and growth and interact with mitochondrial function. Our results suggest that differential non‐random introgression for a subset of loci may be driven by selection favouring the inheritance of compatible mitochondrial and nuclear‐encoded genes in hybrids. -
Baldauf, Sandra (Ed.)Abstract The southwestern and central United States serve as an ideal region to test alternative hypotheses regarding biotic diversification. Genomic data can now be combined with sophisticated computational models to quantify the impacts of paleoclimate change, geographic features, and habitat heterogeneity on spatial patterns of genetic diversity. In this study, we combine thousands of genotyping-by-sequencing (GBS) loci with mtDNA sequences (ND1) from the Texas horned lizard (Phrynosoma cornutum) to quantify relative support for different catalysts of diversification. Phylogenetic and clustering analyses of the GBS data indicate support for at least three primary populations. The spatial distribution of populations appears concordant with habitat type, with desert populations in AZ and NM showing the largest genetic divergence from the remaining populations. The mtDNA data also support a divergent desert population, but other relationships differ and suggest mtDNA introgression. Genotype–environment association with bioclimatic variables supports divergence along precipitation gradients more than along temperature gradients. Demographic analyses support a complex history, with introgression and gene flow playing an important role during diversification. Bayesian multispecies coalescent analyses with introgression (MSci) analyses also suggest that gene flow occurred between populations. Paleo-species distribution models support two southern refugia that geographically correspond to contemporary lineages. We find that divergence times are underestimated and population sizes are overestimated when introgression occurred and is ignored in coalescent analyses, and furthermore, inference of ancient introgression events and demographic history is sensitive to inclusion of a single recently admixed sample. Our analyses cannot refute the riverine barrier or glacial refugia hypotheses. Results also suggest that populations are continuing to diverge along habitat gradients. Finally, the strong evidence of admixture, gene flow, and mtDNA introgression among populations suggests that P. cornutum should be considered a single widespread species under the General Lineage Species Concept.more » « less
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Abstract Surprising social complexity and variability have recently been documented in several mammalian species once believed to be strictly solitary, and variation in resource abundance may drive this variation in sociality. Wagner et al. (Wagner, A. P., S. Creel, L. G. Frank, and S. T. Kalinowski. 2007. Patterns of relatedness and parentage in an asocial, polyandrous striped hyena population. Molecular Ecology 16:4356–4369) reported unusual space-use patterns among female striped hyenas (Hyaena hyaena) in central Kenya, where pairwise relatedness among females increased with the geographic distance separating them. The authors suggested that this pattern, very rare among mammals, might reflect attempts by females to avoid competition with close relatives for scarce resources in areas of range overlap. Here, we compare those data to new data, documenting genetic relatedness and space use in a previously unstudied wild population of striped hyenas in southern Kenya. We tested hypotheses suggesting that resource abundance and population density affect patterns of genetic relatedness and geographic distance in this species. Our results suggest that higher per capita prey density results in relaxed competition for food, and greater social tolerance among female striped hyenas. An hypothesis suggesting lower population density in the southern population was not supported. Relaxed resource competition may also lead to female–female cooperation in the southern population; we documented for the first time behavioral evidence of den sharing by adult female striped hyenas. Our data indicate that different populations of this little-studied species exhibit behavioral plasticity, in this case, markedly different space-use patterns and patterns of spatial relatedness under different ecological conditions.more » « less
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Abstract Background The increasing number of chromosome-level genome assemblies has advanced our knowledge and understanding of macroevolutionary processes. Here, we introduce the genome of the desert horned lizard, Phrynosoma platyrhinos, an iguanid lizard occupying extreme desert conditions of the American southwest. We conduct analysis of the chromosomal structure and composition of this species and compare these features across genomes of 12 other reptiles (5 species of lizards, 3 snakes, 3 turtles, and 1 bird).
Findings The desert horned lizard genome was sequenced using Illumina paired-end reads and assembled and scaffolded using Dovetail Genomics Hi-C and Chicago long-range contact data. The resulting genome assembly has a total length of 1,901.85 Mb, scaffold N50 length of 273.213 Mb, and includes 5,294 scaffolds. The chromosome-level assembly is composed of 6 macrochromosomes and 11 microchromosomes. A total of 20,764 genes were annotated in the assembly. GC content and gene density are higher for microchromosomes than macrochromosomes, while repeat element distributions show the opposite trend. Pathway analyses provide preliminary evidence that microchromosome and macrochromosome gene content are functionally distinct. Synteny analysis indicates that large microchromosome blocks are conserved among closely related species, whereas macrochromosomes show evidence of frequent fusion and fission events among reptiles, even between closely related species.
Conclusions Our results demonstrate dynamic karyotypic evolution across Reptilia, with frequent inferred splits, fusions, and rearrangements that have resulted in shuffling of chromosomal blocks between macrochromosomes and microchromosomes. Our analyses also provide new evidence for distinct gene content and chromosomal structure between microchromosomes and macrochromosomes within reptiles.
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Abstract Species often experience spatial environmental heterogeneity across their range, and populations may exhibit signatures of adaptation to local environmental characteristics. Other population genetic processes, such as migration and genetic drift, can impede the effects of local adaptation. Genetic drift in particular can have a pronounced effect on population genetic structure during large‐scale geographic expansions, where a series of founder effects leads to decreases in genetic variation in the direction of the expansion. Here, we explore the genetic diversity of a desert lizard that occupies a wide range of environmental conditions and that has experienced post‐glacial expansion northwards along two colonization routes. Based on our analyses of a large SNP data set, we find evidence that both climate and demographic history have shaped the genetic structure of populations. Pronounced genetic differentiation was evident between populations occupying cold versus hot deserts, and we detected numerous loci with significant associations with climate. The genetic signal of founder effects, however, is still present in the genomes of the recently expanded populations, which comprise subsets of genetic variation found in the southern populations.
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Abstract Around the world, many species are confined to “Sky Islands,” with different populations in isolated patches of montane habitat. How does this pattern arise? One scenario is that montane species were widespread in lowlands when climates were cooler, and were isolated by local extinction caused by warming conditions. This scenario implies that many montane species may be highly susceptible to anthropogenic warming. Here, we test this scenario in a montane lizard (
Sceloporus jarrovii ) from the Madrean Sky Islands of southeastern Arizona. We combined data from field surveys, climate, population genomics, and physiology. Overall, our results support the hypothesis that this species' current distribution is explained by local extinction caused by past climate change. However, our results for this species differ from simple expectations in several ways: (a) their absence at lower elevations is related to warm winter temperatures, not hot summer temperatures; (b) they appear to exclude a low‐elevation congener from higher elevations, not the converse; (c) they are apparently absent from many climatically suitable but low mountain ranges, seemingly “pushed off the top” by climates even warmer than those today; (d) despite the potential for dispersal among ranges during recent glacial periods (~18,000 years ago), populations in different ranges diverged ~4.5–0.5 million years ago and remained largely distinct; and (e) body temperatures are inversely related to climatic temperatures among sites. These results may have implications for many other Sky Island systems. More broadly, we suggest that Sky Island species may be relevant for predicting responses to future warming. -
Abstract The study of recently diverged lineages whose geographical ranges come into contact can provide insight into the early stages of speciation and the potential roles of reproductive isolation in generating and maintaining species. Such insight can also be important for understanding the strategies and challenges for delimiting species within recently diverged species complexes. Here, we use mitochondrial and nuclear genetic data to study population structure, gene flow and demographic history across a geographically widespread rattlesnake clade, the western rattlesnake species complex (Crotalus cerberus, Crotalus viridis, Crotalus oreganus and relatives), which contains multiple lineages with ranges that overlap geographically or contact one another. We find evidence that the evolutionary history of this group does not conform to a bifurcating tree model and that pervasive gene flow has broadly influenced patterns of present-day genetic diversity. Our results suggest that lineage diversity has been shaped largely by drift and divergent selection in isolation, followed by secondary contact, in which reproductive isolating mechanisms appear weak and insufficient to prevent introgression, even between anciently diverged lineages. The complexity of divergence and secondary contact with gene flow among lineages also provides new context for why delimiting species within this complex has been difficult and contentious historically.