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Hybrid zones are dynamic systems where natural selection, sexual selection, and other evolutionary forces can act on reshuffled combinations of distinct genomes. The movement of hybrid zones, individual traits, or both are of particular interest for understanding the interplay between selective processes. In a hybrid zone involving two lek-breeding birds, secondary sexual plumage traits of Manacus vitellinus, including bright yellow collar and olive belly color, have introgressed ~50 km asymmetrically across the genomic center of the zone into populations more genetically similar to Manacus candei. Males with yellow collars are preferred by females and are more aggressive than parental M. candei, suggesting that sexual selection was responsible for the introgression of male traits. We assessed the spatial and temporal dynamics of this hybrid zone using historical (1989-1994) and contemporary (2017-2020) transect samples to survey both morphological and genetic variation. Genome-wide single nucleotide polymorphism data and several male phenotypic traits show that the genomic center of the zone has remained spatially stable, whereas the olive belly color of male M. vitellinus has continued to introgress over this time period. Our data suggest that sexual selection can continue to shape phenotypes dynamically, independent of a stable genomic transition between species., (Published by Oxford University Press for The Society for the Study of Evolution (SSE) 2024.)

Since the pioneering work of Dobzhansky in the 1930s and 1940s, many chromosomal inversions have been identified, but how they contribute to adaptation remains poorly understood. In Drosophila melanogaster, the widespread inversion polymorphism In(3R)Payne underpins latitudinal clines in fitness traits on multiple continents. Here, we use single-individual whole-genome sequencing, transcriptomics, and published sequencing data to study the population genomics of this inversion on four continents: in its ancestral African range and in derived populations in Europe, North America, and Australia. Our results confirm that this inversion originated in sub-Saharan Africa and subsequently became cosmopolitan; we observe marked monophyletic divergence of inverted and noninverted karyotypes, with some substructure among inverted chromosomes between continents. Despite divergent evolution of this inversion since its out-of-Africa migration, derived non-African populations exhibit similar patterns of long-range linkage disequilibrium between the inversion breakpoints and major peaks of divergence in its center, consistent with balancing selection and suggesting that the inversion harbors alleles that are maintained by selection on several continents. Using RNA-sequencing, we identify overlap between inversion-linked single-nucleotide polymorphisms and loci that are differentially expressed between inverted and noninverted chromosomes. Expression levels are higher for inverted chromosomes at low temperature, suggesting loss of buffering or compensatory plasticity and consistent with higher inversion frequency in warm climates. Our results suggest that this ancestrally tropical balanced polymorphism spread around the world and became latitudinally assorted along similar but independent climatic gradients, always being frequent in subtropical/tropical areas but rare or absent in temperate climates., (© The Author(s) 2023. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution.)

Natural hybrid zones have provided important insights into the evolutionary process, and their geographic dynamics over time can help to disentangle the underlying biological processes that maintain them. Here, we leverage replicated sampling of an identical transect across the hybrid zone between yellow-shafted and red-shafted flickers in the Great Plains to assess its stability over ∼60 years (1955-1957 to 2016-2018). We identify a ∼73-km westward shift in the hybrid zone center toward the range of the red-shafted flicker, but find no associated changes in width over our sampling period. In fact, the hybrid zone remains remarkably narrow, suggesting some kind of selective pressure maintains the zone. By comparing to previous work in the same geographic region, it appears likely that the movement in the hybrid zone has occurred in the years since the early 1980s. This recent movement may be related to changes in climate or land management practices that have allowed westward movement of yellow-shafted flickers into the Great Plains., (© 2022 The Authors. Evolution © 2022 The Society for the Study of Evolution.)

Genetic variation is the fuel of evolution, with standing genetic variation especially important for short-term evolution and local adaptation. To date, studies of spatiotemporal patterns of genetic variation in natural populations have been challenging, as comprehensive sampling is logistically difficult, and sequencing of entire populations costly. Here, we address these issues using a collaborative approach, sequencing 48 pooled population samples from 32 locations, and perform the first continent-wide genomic analysis of genetic variation in European Drosophila melanogaster. Our analyses uncover longitudinal population structure, provide evidence for continent-wide selective sweeps, identify candidate genes for local climate adaptation, and document clines in chromosomal inversion and transposable element frequencies. We also characterize variation among populations in the composition of the fly microbiome, and identify five new DNA viruses in our samples., (© The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.)

Adaptive divergence and speciation may happen despite opposition by gene flow. Identifying the genomic basis underlying divergence with gene flow is a major task in evolutionary genomics. Most approaches (e.g., outlier scans) focus on genomic regions of high differentiation. However, not all genomic architectures potentially underlying divergence are expected to show extreme differentiation. Here, we develop an approach that combines hybrid zone analysis (i.e., focuses on spatial patterns of allele frequency change) with system-specific simulations to identify loci inconsistent with neutral evolution. We apply this to a genome-wide SNP set from an ideally suited study organism, the intertidal snail Littorina saxatilis , which shows primary divergence between ecotypes associated with different shore habitats. We detect many SNPs with clinal patterns, most of which are consistent with neutrality. Among non-neutral SNPs, most are located within three large putative inversions differentiating ecotypes. Many non-neutral SNPs show relatively low levels of differentiation. We discuss potential reasons for this pattern, including loose linkage to selected variants, polygenic adaptation and a component of balancing selection within populations (which may be expected for inversions). Our work is in line with theory predicting a role for inversions in divergence, and emphasizes that genomic regions contributing to divergence may not always be accessible with methods purely based on allele frequency differences. These conclusions call for approaches that take spatial patterns of allele frequency change into account in other systems.

Clines in chromosomal inversion polymorphisms-presumably driven by climatic gradients-are common but there is surprisingly little evidence for selection acting on them. Here we address this long-standing issue in Drosophila melanogaster by using diagnostic single nucleotide polymorphism (SNP) markers to estimate inversion frequencies from 28 whole-genome Pool-seq samples collected from 10 populations along the North American east coast. Inversions In(3L)P, In(3R)Mo, and In(3R)Payne showed clear latitudinal clines, and for In(2L)t, In(2R)NS, and In(3R)Payne the steepness of the clinal slopes changed between summer and fall. Consistent with an effect of seasonality on inversion frequencies, we detected small but stable seasonal fluctuations of In(2R)NS and In(3R)Payne in a temperate Pennsylvanian population over 4 years. In support of spatially varying selection, we observed that the cline in In(3R)Payne has remained stable for >40 years and that the frequencies of In(2L)t and In(3R)Payne are strongly correlated with climatic factors that vary latitudinally, independent of population structure. To test whether these patterns are adaptive, we compared the amount of genetic differentiation of inversions versus neutral SNPs and found that the clines in In(2L)t and In(3R)Payne are maintained nonneutrally and independent of admixture. We also identified numerous clinal inversion-associated SNPs, many of which exhibit parallel differentiation along the Australian cline and reside in genes known to affect fitness-related traits. Together, our results provide strong evidence that inversion clines are maintained by spatially-and perhaps also temporally-varying selection. We interpret our data in light of current hypotheses about how inversions are established and maintained., (© The Author 2016. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.)

Uncovering the genetic basis of phenotypic variation and the population history under which it established is key to understand the trajectories along which local adaptation evolves. Here, we investigated the genetic basis and evolutionary history of a clinal plumage color polymorphism in European barn owls (Tyto alba). Our results suggest that barn owls colonized the Western Palearctic in a ring-like manner around the Mediterranean and meet in secondary contact in Greece. Rufous coloration appears to be linked to a recently evolved nonsynonymous-derived variant of the melanocortin 1 receptor (MC1R) gene, which according to quantitative genetic analyses evolved under local adaptation during or following the colonization of Central Europe. Admixture patterns and linkage disequilibrium between the neutral genetic background and color found exclusively within the secondary contact zone suggest limited introgression at secondary contact. These results from a system reminiscent of ring species provide a striking example of how local adaptation can evolve from derived genetic variation., (© 2015 The Author(s). Evolution © 2015 The Society for the Study of Evolution.)

Local adaptation and sexual dimorphism are iconic evolutionary scenarios of intraspecific adaptive differentiation in the face of gene flow. Although theory has traditionally considered local adaptation and sexual dimorphism as conceptually distinct processes, emerging data suggest that they often act concurrently during evolutionary diversification. Here, I merge theories of local adaptation in space and sex-specific adaptation over time, and show that their confluence yields several new predictions about the roles of context-specific selection, migration, and genetic correlations, in adaptive diversification. I specifically revisit two influential predictions from classical studies of clinal adaptation and sexual dimorphism: (1) that local adaptation should decrease with distance from the species' range center and (2) that opposing directional selection between the sexes (sexual antagonism) should inevitably accompany the evolution of sexual dimorphism. I show that both predictions can break down under clinally varying selection. First, the geography of local adaptation can be sexually dimorphic, with locations of relatively high local adaptation differing profoundly between the sexes. Second, the intensity of sexual antagonism varies across the species' range, with subpopulations near the range center representing hotspots for antagonistic selection. The results highlight the context-dependent roles of migration versus sexual conflict as primary constraints to adaptive diversification., (© 2015 The Author(s). Evolution © 2015 The Society for the Study of Evolution.)

In this article, we couple the geographic variation in 127 single-nucleotide polymorphism (SNP) frequencies in genes of 46 enzymes of central metabolism with their associated cis-expression variation to predict latitudinal or climatic-driven gene expression changes in the metabolic architecture of Drosophila melanogaster. Forty-two percent of the SNPs in 65% of the genes show statistically significant clines in frequency with latitude across the 20 local population samples collected from southern Florida to Ontario. A number of SNPs in the screened genes are also associated with significant expression variation within the Raleigh population from North Carolina. A principal component analysis of the full variance-covariance matrix of latitudinal changes in SNP-associated standardized gene expression allows us to identify those major genes in the pathway and its associated branches that are likely targets of natural selection. When embedded in a central metabolic context, we show that these apparent targets are concentrated in the genes of the upper glycolytic pathway and pentose shunt, those controlling glycerol shuttle activity, and finally those enzymes associated with the utilization of glutamate and pyruvate. These metabolites possess high connectivity and thus may be the points where flux balance can be best shifted. We also propose that these points are conserved points associated with coupling energy homeostasis and energy sensing in mammals. We speculate that the modulation of gene expression at specific points in central metabolism that are associated with shifting flux balance or possibly energy-state sensing plays a role in adaptation to climatic variation., (© The Author 2014. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.)

Understanding how natural environments shape phenotypic variation is a major aim in evolutionary biology. Here, we have examined clinal, likely genetically based variation in morphology among 19 populations of the fruit fly (Drosophila melanogaster) from Africa and Europe, spanning a range from sea level to 3000 m altitude and including locations approximating the southern and northern range limit. We were interested in testing whether latitude and altitude have similar phenotypic effects, as has often been postulated. Both latitude and altitude were positively correlated with wing area, ovariole number, and cell number. In contrast, latitude and altitude had opposite effects on the ratio between ovariole number and body size, which was negatively correlated with egg production rate per ovariole. We also used transgenic manipulation to examine how increased cell number affects morphology and found that larger transgenic flies, due to a higher number of cells, had more ovarioles, larger wings, and, unlike flies from natural populations, increased wing loading. Clinal patterns in morphology are thus not a simple function of changes in body size; instead, each trait might be subject to different selection pressures. Together, our results provide compelling evidence for profound similarities as well as differences between phenotypic effects of latitude and altitude., (© 2014 The Author(s). Evolution © 2014 The Society for the Study of Evolution.)

Evolution of a new gene function is a fundamental process of adaptation. Gene duplication followed by divergence due to relaxed selection on redundant copies has been viewed as the predominant mechanism involved in this process. At a macroevolutionary scale, evidence for this scenario came from the analysis of sequences of genes families. However, even if several genetic models have described the different potential microevolutionary scenario for a new function to evolve, little is really known about the initial evolutionary dynamics of such processes. We analyze such early dynamics in natural populations of the mosquito Culex pipiens polymorphic for a duplication at Ace.1, a locus involved in insecticide resistance. The date of occurrence and the selective advantages of the duplication were estimated using frequency data. We propose a scenario where the spread of a duplication is driven, from the very beginning, by selection due to insecticide treatment., (© 1998 The Society for the Study of Evolution.)

The introgression pattern of centromeric nucleolar organizer regions (NORs) was studied in house mice from the hybrid zone between Mus musculus musculus and Mus musculus domesticus in Denmark. In this region, the two subspecies are chromosomally differentiated: M. m domesticus carries three pairs of Robertsonian (Rb) fusion chromosomes (2n = 34), while M. m. musculus exhibits the ancestral karyotype of 2n = 40 acrocentric chromosomes. A previous chromosomal analysis showed that the Rb clines were staggered and nonconcordant, and that the Rb fusions did not introgress into the M. m. musculus genome due to incompatibilities involving only the centromeric regions. In the present study, the distribution of a centromeric NOR cluster located on an acrocentric chromosome not involved in the Rb fusions (chromosome 11; NOR 11 ) was investigated to determine if the observed centromeric incompatibilities were limited to the chromosomal rearrangements or were related to centromeric differentiation between the subspecies. The cytogenetic study by silver staining documented the activity pattern of the five major NOR-bearing chromosome pairs (12, 15, 16, 18, and 19) common to both subspecies and confirmed presence of NOR 11 in M. m. musculus and absence in M. m. domesticus. The NOR 11 activity pattern showed a very narrow and off-centered clinal transition. An in situ hybridization analysis with rDNA probes indicated that the decrease in frequency of activity of NOR 11 through the hybrid zone was related to absence of ribosomal genes in this cluster and not to transcription repression due to competitive or dominance interactions. The center of the NOR 11 cline was significantly different from that of the consensus allozymic markers, but coincided with that of the steepest Rb cline. Several arguments support the view that the selective processes involved in maintaining the NOR 11 cline are related to the centromeric region of these chromosomes. These include: (1) the similarity in shape and position of the Rb and NOR 11 clines; (2) the absence of activity dysfunction involving NOR 11 ; and (3) the tight linkage between NORs and centromeres in house mice. This study indicates that the centromeric segments of acrocentric chromosomes not involved in chromosomal rearrangements show incompatibilities similar to those evidenced by the Rb fusions. These centromeric incompatibilities are thus more likely related to centromeric origin and subspecific differentiation (domesticus vs. musculus) than to centromeric rearrangement (Rb vs. non-Rb). In this case, it may be predicted that the selective processes maintaining the chromosomal clines are distributed over many, if not all, the centromeres and may combine . to limit the gene flow between M. m. domesticus and M. m. musculus., (© 1998 The Society for the Study of Evolution.)

Dobzhansky's model of epistatic selection assumes that viable genotypes form "clusters" in genotype space so that populations can evolve from one state to a reproductively isolated state following a "ridge" of well-fit genotypes without crossing any deep adaptive valleys. Recently, the importance of Dobzhansky-type models in evolutionary studies has been reemphasized by Gavrilets (1997a) and Gavrilets and Gravner (1997) who argue that the existence of "ridges" of well-fit genotypes connecting reproductively isolated genotypes is actually a general property of multidimensional adaptive landscapes. Using rigorous techniques and numerical simulations, I analyze clines in the frequencies of selected and neutral alleles maintained by a balance of migration and Dobzhansky-type epistatic selection acting on two diallelic loci. I show that Dobzhansky-type epistatic selection can build up a very strong barrier to neutral gene flow. I describe properties of clines that are indicative of Dobzhansky-type selection., (© 1997 The Society for the Study of Evolution.)

We investigate the interplay between gene flow and adaptation in peripheral populations of a widespread species. Models are developed for the evolution of a quantitative trait under clinally varying selection in a species whose density decreases from the center of the range to its periphery. Two major results emerge. First, gene flow from populations at the range center can be a strong force that inhibits peripheral populations from evolving to their local ecological optima. As a result, peripheral populations experience persistent directional selection. Second, response to local selection pressures can cause rapid and substantial evolution when a peripheral population is isolated from gene flow. The amount of evolutionary change depends on gene flow, selection, the ecological gradient, and the trait's heritability. Rapid divergence can also occur between the two halves of a formerly continuous population that is divided by a vicariant event. A general conclusion is that disruption of gene flow can cause evolutionary divergence, perhaps leading to speciation, in the absence of contributions from random genetic drift., (© 1997 The Society for the Study of Evolution.)

Fisher's method of junctions is used to investigate the degree of association between selected alleles in a cline, in the limit where there is divergence between very many genes. A computer model is used to simulate one of a pair of infinite demes that exchange individuals each generation. Selection is on haploids; it is additive and is equivalent to heterozygote disadvantage. Recombination is uniform over a single chromosome. A "critical value" of selection exists at equilibrium, below which loci act independently and above which they act in association (Barton 1983). Starting with secondary contact, simulation results contrast markedly with the equilibrium solution. The "critical value" is not apparent in the simulated clines, even after many generations. Rather, loci remain associated to some extent under all degrees of selection. The simulation is consistent with the equilibrium analysis in all other respects, and therefore indicates that under weak selection the approach to equilibrium is very slow. This is borne out by further numerical calculations. The slow approach to equilibrium enables us to estimate the time since contact between two demes under idealized conditions. Extending this work toward natural hybrid zones is discussed., (© 1995 The Society for the Study of Evolution.)

Two parapatric chromosomal races of the common shrew (Sorex araneus) in Poland differ in their complement of metacentric arm combinations: hk, io, gr, nm (race IV), and hi, ko, gm, np (race II). In hybrids, these eight race-diagnostic metacentrics form two randomly segregating complexes. The first complex (C 1 ) occurs in the form of a ring configuration ok/kh/hi/io, or a chain o/ok/kh/hi/i (when there is Robertsonian polymorphism of the element io). The second complex (C 2 ) always takes the form of a six-element chain configuration r/rg/gm/mn/np/p. The C 2 complex may be shortened to five or even four elements, when acrocentrics g, m and n are present. In the contact zone we found shrews of pure races (race II or IV), as well as hybrids with C 1 or C 2 complexes, and recombinants hi, ko, gr, nm. Complex heterozygotes are likely to suffer reduced fertility due to malsegregation at meiosis. However, the C 1 hybrids with ring configurations occur with a high frequency throughout the contact zone. This suggest that their fitness is only slightly lowered relative to pure race individuals, in contrast to the hybrids with C 1 or C 2 chain configurations, which presumably have a more heavily reduced fertility. On the other hand, at the center of the zone there is a high proportion of recombinants, which, being chromosomal homozygotes, should display normal meiotic segregation. Furthermore, the high frequencies of recombinants within the contact zone should facilitate gene flow between the races. The occurrence of recombinants plays a similar role as the appearance of the maximum frequencies of acrocentric homozygotes described in several contact zones of S. araneus., (© 1991 The Society for the Study of Evolution.)