Kira E. Delmore

Dramatic intraspecific differences in migratory routes, stopover sites and wintering areas, revealed using light-level geolocators

Migratory divides are contact zones between breeding populations that use divergent migratory routes and have been described in a variety of species. These divides are of major importance to evolution, ecology and conservation but have been identified using limited band recovery data and/or indirect methods. Data from band recoveries and mitochondrial haplotypes suggested that inland and coastal Swainsons thrushes (Catharus ustulatus) form a migratory divide in western North America. We attached light-level geolocators to birds at the edges of this contact zone to provide, to our knowledge, the first direct test of a putative divide using data from individual birds over the entire annual cycle. Coastal thrushes migrated along the west coast to Mexico, Guatemala and Honduras. Some of these birds used multiple wintering sites. Inland thrushes migrated across the Rocky Mountains, through central North America to Columbia and Venezuela. These birds migrated longer distances than coastal birds and performed a loop migration, navigating over the Gulf of Mexico in autumn and around this barrier in spring. These findings support the suggestion that divergent migratory behaviour could contribute to reproductive isolation between migrants, advance our understanding of their non-breeding ecology, and are integral to development of detailed conservation strategies for this group.

Hybrid songbirds employ intermediate routes in a migratory divide

Migratory divides are contact zones between populations that use different routes to navigate around unsuitable areas on seasonal migration. Hybrids in divides have been predicted to employ intermediate and potentially inferior routes. We provide the first direct test of this hypothesis, using light-level geolocators to track birds breeding in a hybrid zone between Swainsons thrushes in western Canada. Compared to parental forms, hybrids exhibited increased variability in their migratory routes, with some using intermediate routes that crossed arid and mountainous regions, and some using the same routes as one parental group on fall migration and the other on spring migration. Hybrids also tended to use geographically intermediate wintering sites. Analysis of genetic variation across the hybrid zone suggests moderately strong selection against hybrids. These results indicate that seasonal migratory behaviour might be a source of selection against hybrids, supporting a possible role for migration in speciation.

Genomic analysis of a migratory divide reveals candidate genes for migration and implicates selective sweeps in generating islands of differentiation

Differential gene flow, reductions in diversity following linked selection and/or features of the genome can structure patterns of genomic differentiation during the process of speciation. Possible sources of reproductive isolation are well studied between coastal and inland subspecies groups of Swainsons thrushes, with differences in seasonal migratory behaviour likely playing a key role in reducing hybrid fitness. We assembled and annotated a draft reference genome for this species and generated whole‐genome shotgun sequence data for populations adjacent to the hybrid zone between these groups. We documented substantial genomewide heterogeneity in relative estimates of genetic differentiation between the groups. Within population diversity was lower in areas of high relative differentiation, supporting a role for selective sweeps in generating this pattern. Absolute genetic differentiation was reduced in these areas, further suggesting that recurrent selective sweeps in the ancestral population and/or between divergent populations following secondary contact likely occurred. Relative genetic differentiation was also higher near centromeres and on the Z chromosome, suggesting that features of the genome also contribute to genomewide heterogeneity. Genes linked to migratory traits were concentrated in islands of differentiation, supporting previous suggestions that seasonal migration is under divergent selection between Swainsons thrushes. Differences in migratory behaviour likely play a central role in the speciation of many taxa; we developed the infrastructure here to permit future investigations into the role several candidate genes play in reducing gene flow between not only Swainsons thrushes but other species as well.

Recurrent selection explains parallel evolution of genomic regions of high relative but low absolute differentiation in a ring species

Recent technological developments allow investigation of the repeatability of evolution at the genomic level. Such investigation is particularly powerful when applied to a ring species, in which spatial variation represents changes during the evolution of two species from one. We examined genomic variation among three subspecies of the greenish warbler ring species, using genotypes at 13 013 950 nucleotide sites along a new greenish warbler consensus genome assembly. Genomic regions of low within‐group variation are remarkably consistent between the three populations. These regions show high relative differentiation but low absolute differentiation between populations. Comparisons with outgroup species show the locations of these peaks of relative differentiation are not well explained by phylogenetically conserved variation in recombination rates or selection. These patterns are consistent with a model in which selection in an ancestral form has reduced variation at some parts of the genome, and those same regions experience recurrent selection that subsequently reduces variation within each subspecies. The degree of heterogeneity in nucleotide diversity is greater than explained by models of background selection, but is consistent with selective sweeps. Given the evidence that greenish warblers have had both population differentiation for a long period of time and periods of gene flow between those populations, we propose that some genomic regions underwent selective sweeps over a broad geographic area followed by within‐population selection‐induced reductions in variation. An important implication of this ‘sweep‐before‐differentiation’ model is that genomic regions of high relative differentiation may have moved among populations more recently than other genomic regions.

Gene flow and selection interact to promote adaptive divergence in regions of low recombination

Adaptation to new environments often occurs in the face of gene flow. Under these conditions, gene flow and recombination can impede adaptation by breaking down linkage disequilibrium between locally adapted alleles. Theory predicts that this decay can be halted or slowed if adaptive alleles are tightly linked in regions of low recombination, potentially favouring divergence and adaptive evolution in these regions over others. Here, we compiled a global genomic data set of over 1,300 individual threespine stickleback from 52 populations and compared the tendency for adaptive alleles to occur in regions of low recombination between populations that diverged with or without gene flow. In support of theory, we found that putatively adaptive alleles (FST and dXY outliers) tend to occur more often in regions of low recombination in populations where divergent selection and gene flow have jointly occurred. This result remained significant when we employed different genomic window sizes, controlled for the effects of mutation rate and gene density, controlled for overall genetic differentiation, varied the genetic map used to estimate recombination and used a continuous (rather than discrete) measure of geographic distance as proxy for gene flow/shared ancestry. We argue that our study provides the first statistical evidence that the interaction of gene flow and selection biases divergence toward regions of low recombination.

Population genetics and abundance of the Endangered grey-headed lemur Eulemur cinereiceps in south-east Madagascar: assessing risks for fragmented and continuous populations

Knowledge of both population size and genetic diversity is critical for assessing extinction risk but few studies include concurrent estimates of these two compo- nents of population biology. We conducted an investigation of population density and size, and genetic variation and past demographic events, of the Endangered grey-headed lemur Eulemur cinereiceps in south-east Madagascar. We estimated lemur density using line-transect surveys and used satellite imagery to calculate forest fragment area in three localities. We collected tissue samples from 53 individuals and used 26 polymorphic microsatellite loci to obtain measures of population structure (divergence and diversity) across these localities. We tested the probability of past bottleneck events using three models. Contrary to expecta- tion, there were no significant differences in population density across localities. Genetic diversity decreased, but not significantly, with decreasing habitat area and population size. We found a higher likelihood of past bottleneck events in the fragmented coastal populations. The low population size and prior decline in diversity in coastal patches are consistent with their isolation, anthropogenic disturbance, and exposure to cyclone activity. The similarities in the estimates of density between continuous and fragmented sites may indicate recent population growth in the frag- ments but these populations nevertheless remain at risk from reduced levels of genetic variation. These patterns should be confirmed with more extensive sampling across the limited range of E. cinereiceps.

Morphological characterization of a brown lemur hybrid zone (Eulemur rufifrons × E. cinereiceps)

Hybridization has recently been identified as a pervasive force in the evolution of primates. In this study, we characterized a hybrid zone between two species of brown lemur (Eulemur rufifrons and E. cinereiceps) in the Andringitra region of southeastern Madagascar using morphological traits. We immobilized animals along a north-south transect (∼80 km), scored them for their degree of hybridity using pelage traits and measured standard morphometric variables. Results from our study suggest that hybridization between E. rufifrons and E. cinereiceps is extensive, with the hybrid zone extending over 42.6 km and being composed mostly of later generation hybrids. We also identified significant variation between ancestral groups in our study: hybrid males exhibited longer tails than both parental species and sexual dimorphism in upper canine height favoring males was documented in E. rufifrons. These patterns could suggest that gene flow between parental and hybrid populations is relatively limited. Finally, significant differences between ancestral groups in relative body mass and skin-fold thickness were absent in our study, indicating that, as measured by these proxies, hybrids are equally as fit as parental forms. Based on these preliminary findings, the Andringitra hybrid zone could conform to the bounded superiority model of hybrid zone stability (i.e., it could be being maintained by selection favoring hybrids within transitional habitats). Accordingly, hybrids in Andringitra may be an unusual case among primates, representing a stable recombinant but distinct lineage. This conclusion has important implications for evolutionary processes within the brown lemur species complex.

Phenotypic divergence during speciation is inversely associated with differences in seasonal migration.

Differences in seasonal migration might promote reproductive isolation and differentiation by causing populations in migratory divides to arrive on the breeding grounds at different times and/or produce hybrids that take inferior migratory routes. We examined this question by quantifying divergence in song, colour, and morphology between sister pairs of North American migratory birds. We predicted that apparent rates of phenotypic differentiation would differ between pairs that do and do not form migratory divides. Consistent with this prediction, results from mixed effects models and Ornstein–Uhlenbeck models of evolution showed different rates of divergence between these groups; surprisingly, differentiation was greater among non-divide pairs. We interpret this finding as a result of variable rates of population blending and fusion between partially diverged forms. Ancient pairs of populations that subsequently fused are now observed as a single form, whereas those that did not fuse are observable as pairs and included in our study. We propose that fusion of two populations is more likely to occur when they have similar migratory routes and little other phenotypic differentiation that would cause reproductive isolation. By contrast, pairs with migratory divides are more likely to remain reproductively isolated, even when differing little in other phenotypic traits. These findings suggest that migratory differences may be one among several isolating barriers that prevent divergent populations from fusing and thereby increase the likelihood that they will continue differentiating as distinct species.

Clinal variation in a brown lemur (Eulemur spp.) hybrid zone: Combining morphological, genetic and climatic data to examine stability

Studies of hybrid zones can inform our understanding of reproductive isolation and speciation. Two species of brown lemur (Eulemur rufifrons and E. cinereiceps) form an apparently stable hybrid zone in the Andringitra region of south‐eastern Madagascar. The aim of this study was to identify factors that contribute to this stability. We sampled animals at 11 sites along a 90‐km transect through the hybrid zone and examined variation in 26 microsatellites, the D‐loop region of mitochondrial DNA, six pelage and nine morphological traits; we also included samples collected in more distant allopatric sites. Clines in these traits were noncoincident, and there was no increase in either inbreeding coefficients or linkage disequilibrium at the centre of the zone. These results could suggest that the hybrid zone is maintained by weak selection against hybrids, conforming to either the tension zone or geographical selection‐gradient model. However, a closer examination of clines in pelage and microsatellites indicates that these clines are not sigmoid or stepped in shape but instead plateau at their centre. Sites within the hybrid zone also occur in a distinct habitat, characterized by greater seasonality in precipitation and lower seasonality in temperature. Together, these findings suggest that the hybrid zone may follow the bounded superiority model, with exogenous selection favouring hybrids within the transitional zone. These findings are noteworthy, as examples supporting the bounded superiority model are rare and may indicate a process of ecologically driven speciation without geographical isolation.

Investigating Factors that Generate and Maintain Variation in Migratory Orientation: A Primer for Recent and Future Work

The amazing accuracy of migratory orientation performance across the animal kingdom is facilitated by the use of magnetic and celestial compass systems that provide individuals with both directional and positional information. Quantitative genetics analyses in several animal systems suggests that migratory orientation has a strong genetic component. Nevertheless, the exact identity of genes controlling orientation remains largely unknown, making it difficult to obtain an accurate understanding of this fascinating behavior on the molecular level. Here, we provide an overview of molecular genetic techniques employed thus far, highlight the pros and cons of various approaches, generalize results from species-specific studies whenever possible, and evaluate how far the field has come since early quantitative genetics studies. We emphasize the importance of examining different levels of molecular control, and outline how future studies can take advantage of high-resolution tracking and sequencing techniques to characterize the genomic architecture of migratory orientation.