Genetic evidence for widespread population size expansion in North American boreal birds prior to the Last Glacial Maximum.

Pleistocene climate cycles are well documented to have shaped contemporary species distributions and genetic diversity. Northward range expansions in response to deglaciation following the Last Glacial Maximum (LGM; approximately 21 000 years ago) are surmised to have led to population size expansions in terrestrial taxa and changes in seasonal migratory behaviour. Recent findings, however, suggest that some northern temperate populations may have been more stable than expected through the LGM. We modelled the demographic history of 19 co-distributed boreal-breeding North American bird species from full mitochondrial gene sets and species-specific molecular rates. We used these demographic reconstructions to test how species with different migratory strategies were affected by glacial cycles. Our results suggest that effective population sizes increased in response to Pleistocene deglaciation earlier than the LGM, whereas genetic diversity was maintained throughout the LGM despite shifts in geographical range. We conclude that glacial cycles prior to the LGM have most strongly shaped contemporary genetic diversity in these species. We did not find a relationship between historic population dynamics and migratory strategy, contributing to growing evidence that major switches in migratory strategy during the LGM are unnecessary to explain contemporary migratory patterns.

Comparative Population Genomics of Cryptic Speciation and Adaptive Divergence in Bicknell's and Gray-Cheeked Thrushes (Aves: Catharus bicknelli and Catharus minimus).

Cryptic speciation may occur when reproductive isolation is recent or the accumulation of morphological differences between sister lineages is slowed by stabilizing selection preventing phenotypic differentiation. In North America, Bicknell's Thrush (Catharus bicknelli) and its sister species, the Gray-cheeked Thrush (Catharus minimus), are parapatrically breeding migratory songbirds, distinguishable in nature only by subtle differences in song and coloration, and were recognized as distinct species only in the 1990s. Previous molecular studies have estimated that the species diverged approximately 120,000-420,000 YBP and found very low levels of introgression despite their similarity and sympatry in the spring (prebreeding) migration. To further clarify the history, genetic divergence, genomic structure, and adaptive processes in C. bicknelli and C. minimus, we sequenced and assembled high-coverage reference genomes of both species and resequenced genomes from population samples of C. bicknelli, C. minimus, and two individuals of the Swainson's Thrush (Catharus ustulatus). The genome of C. bicknelli exhibits markedly higher abundances of transposable elements compared with other Catharus and chicken. Demographic and admixture analyses confirm moderate genome-wide differentiation (Fst ≈ 0.10) and limited gene flow between C. bicknelli and C. minimus, but suggest a more recent divergence than estimates based on mtDNA. We find evidence of rapid evolution of the Z-chromosome and elevated divergence consistent with natural selection on genomic regions near genes involved with neuronal processes in C. bicknelli. These genomes are a useful resource for future investigations of speciation, migration, and adaptation in Catharus thrushes.

Rapid adaptive evolution of northeastern coyotes via hybridization with wolves.

The dramatic expansion of the geographical range of coyotes over the last 90 years is partly explained by changes to the landscape and local extinctions of wolves, but hybridization may also have facilitated their movement. We present mtDNA sequence data from 686 eastern coyotes and measurements of 196 skulls related to their two-front colonization pattern. We find evidence for hybridization with Great Lakes wolves only along the northern front, which is correlated with larger skull size, increased sexual dimorphism and a five times faster colonization rate than the southern front. Northeastern haplotype diversity is low, suggesting that this population was founded by very few females moving across the Saint Lawrence River. This northern front then spread south and west, eventually coming in contact with an expanding front of non-hybrid coyotes in western New York and Pennsylvania. We suggest that hybridization with wolves in Canada introduced adaptive variation that contributed to larger size, which in turn allowed eastern coyotes to better hunt deer, allowing a more rapid colonization of new areas than coyotes without introgressed wolf genes. Thus, hybridization is a conduit by which genetic variation from an extirpated species has been reintroduced into northeastern USA, enabling northeastern coyotes to occupy a portion of the niche left vacant by wolves.

DNA from a 100-year-old holotype confirms the validity of a potentially extinct hummingbird species.

We used mtDNA sequence data to confirm that the controversial 100-year-old holotype of the Bogotá sunangel (Heliangelus zusii) represents a valid species. We demonstrate that H. zusii is genetically well differentiated from taxa previously hypothesized to have given rise to the specimen via hybridization. Phylogenetic analyses place H. zusii as sister to a clade of mid- to high-elevation Andean species currently placed in the genera Taphrolesbia and Aglaiocercus. Heliangelus zusii, presumed extinct, has never been observed in nature by biologists. We infer that the species occupied a restricted distribution between the upper tropical and temperate zones of the northern Andes and that it was most probably driven to extinction by deforestation that accompanied human population growth during the nineteenth and early twentieth centuries. We demonstrate the feasibility of obtaining DNA from nearly microscopic tissue samples from old hummingbird specimens and suggest that these methods could be used to resolve the taxonomy of dozens of avian taxa known only from type specimens.

Drivers of community turnover differ between avian hemoparasite genera along a North American latitudinal gradient.

The latitudinal diversity gradient (LDG) is an established macroecological pattern, but is poorly studied in microbial organisms, particularly parasites. In this study, we tested whether latitude, elevation, and host species predicted patterns of prevalence, alpha diversity, and community turnover of hemosporidian parasites. We expected parasite diversity to decrease with latitude, alongside the diversity of their hosts and vectors. Similarly, we expected infection prevalence to decrease with latitude as vector abundances decrease. Lastly, we expected parasite community turnover to increase with latitudinal distance and to be higher between rather than within host species. We tested these hypotheses by screening blood and tissue samples of three closely related avian species in a clade of North American songbirds (Turdidae: Catharus, n = 466) across 17.5° of latitude. We used a nested PCR approach to identify parasites in hemosporidian genera that are transmitted by different dipteran vectors. Then, we implemented linear-mixed effects and generalized dissimilarity models to evaluate the effects of latitude, elevation, and host species on parasite metrics. We found high diversity of hemosporidian parasites in Catharus thrushes (n = 44 lineages) but no evidence of latitudinal gradients in alpha diversity or prevalence. Parasites in the genus Leucocytozoon were most prevalent and lineage rich in this study system; however, there was limited turnover with latitude and host species. Contrastingly, Plasmodium parasites were less prevalent and diverse than Leucocytozoon parasites, yet communities turned over at a higher rate with latitude and host species. Leucocytozoon communities were skewed by the dominance of one or two highly prevalent lineages with broad latitudinal distributions. The few studies that evaluate the hemosporidian LDG do not find consistent patterns of prevalence and diversity, which makes it challenging to predict how they will respond to global climate change.

Length polymorphisms at two candidate genes explain variation of migratory behaviors in blackpoll warblers (Setophaga striata).

Migratory behaviors such as the timing and duration of migration are genetically inherited and can be under strong natural selection, yet we still know very little about the specific genes or molecular pathways that control these behaviors. Studies in candidate genes Clock and Adcyap1 have revealed that both of these loci can be significantly correlated with migratory behaviors in birds, though observed relationships appear to vary across species. We investigated geographic genetic structure of Clock and Adcyap1 in four populations of blackpoll warblers (Setophaga striata), a Neotropical-Nearctic migrant that exhibits geographic variation in migratory timing and duration across its boreal breeding distribution. Further, we used data on migratory timing and duration, obtained from light-level geolocator trackers to investigate candidate genotype-phenotype relationships at the individual level. While we found no geographic structure in either candidate gene, we did find evidence that candidate gene lengths are correlated with five of the six migratory traits. Maximum Clock allele length was significantly and negatively associated with spring arrival date. Minimum Adcyap1 allele length was significantly and negatively associated with spring departure date and positively associated with fall arrival date at the wintering grounds. Additionally, we found a significant interaction between Clock and Adcyap1 allele lengths on both spring and fall migratory duration. Adcyap1 heterozygotes also had significantly shorter migration duration in both spring and fall compared to homozygotes. Our results support the growing body of evidence that Clock and Adcyap1 allele lengths are correlated with migratory behaviors in birds.

Pair of lice lost or parasites regained: the evolutionary history of anthropoid primate lice.

BACKGROUND: The parasitic sucking lice of primates are known to have undergone at least 25 million years of coevolution with their hosts. For example, chimpanzee lice and human head/body lice last shared a common ancestor roughly six million years ago, a divergence that is contemporaneous with their hosts. In an assemblage where lice are often highly host specific, humans host two different genera of lice, one that is shared with chimpanzees and another that is shared with gorillas. In this study, we reconstruct the evolutionary history of primate lice and infer the historical events that explain the current distribution of these lice on their primate hosts. RESULTS: Phylogenetic and cophylogenetic analyses suggest that the louse genera Pediculus and Pthirus are each monophyletic, and are sister taxa to one another. The age of the most recent common ancestor of the two Pediculus species studied matches the age predicted by host divergence (ca. 6 million years), whereas the age of the ancestor of Pthirus does not. The two species of Pthirus (Pthirus gorillae and Pthirus pubis) last shared a common ancestor ca. 3-4 million years ago, which is considerably younger than the divergence between their hosts (gorillas and humans, respectively), of approximately 7 million years ago. CONCLUSION: Reconciliation analysis determines that there are two alternative explanations that account for the current distribution of anthropoid primate lice. The more parsimonious of the two solutions suggests that a Pthirus species switched from gorillas to humans. This analysis assumes that the divergence between Pediculus and Pthirus was contemporaneous with the split (i.e., a node of cospeciation) between gorillas and the lineage leading to chimpanzees and humans. Divergence date estimates, however, show that the nodes in the host and parasite trees are not contemporaneous. Rather, the shared coevolutionary history of the anthropoid primates and their lice contains a mixture of evolutionary events including cospeciation, parasite duplication, parasite extinction, and host switching. Based on these data, the coevolutionary history of primates and their lice has been anything but parsimonious.

Molecular identification of lice from pre-Columbian mummies.

BACKGROUND: Three distinctly different lineages of head and body lice are known to parasitize humans. One lineage includes head and body lice and is currently worldwide in distribution (type A). The other 2 (types B and C) include only head lice and are geographically restricted. It was hypothesized that head louse phylotypes were exchanged only recently, after European exploration and colonization (after Columbus). METHODS: To determine which louse type or types were found in the Americas before European colonization, we used polymerase chain reaction in 2 laboratories to amplify DNA from 2 genes (Cytb and Cox1) belonging to 1000-year-old lice collected from Peruvian mummies. RESULTS: Only the worldwide type (type A) was found. Therefore, this phylotype was worldwide before European colonization, as type A lice were common in Europe, Africa, and Asia. CONCLUSIONS: The findings of this study show that several phylotypes of head lice have coexisted for centuries in humans and support the claim that type A lice were present in the Americas before the time of Columbus.

Comparative phylogeography and genetic structure of Vanuatu birds: control region variation in a rail, a dove, and a passerine.

We examined variation in mitochondrial control region (Domain I) sequences in three distantly related species of birds found on multiple islands in Vanuatu: the Buff-banded Rail Gallirallus philippensis (n=21, 433bp), the Emerald Dove Chalcophaps indica (n=21, 513bp), and the Streaked Fantail Rhipidura spilodera (n=17, 326bp). Nucleotide and haplotype diversity were similar in all three species and showed little to no geographic structure within Vanuatu. Estimates of demographic parameters, tests for excess rare alleles, and the structure of both haplotype networks and pairwise mismatch distributions support a hypothesis of recent colonization and subsequent expansion in C. indica and R. spilodera but not in G. philippensis. Phylogenetic analyses suggest that G. philippensis samples from Vanuatu are polyphyletic, and further indicate that this species has had a more complex history of colonization than do the other two species. Estimated divergence times of alleles sampled in Vanuatu suggest there may be slight differences among species in the timing of colonization of Vanuatu despite differences in flight ability and presumed dispersal ability. In all three species, current populations probably derive from colonists that arrived several million years after the islands formed. Our comparisons illustrate the potential of direct genetic analyses of to highlight historical differences among co-distributed species with similar levels of phenotypic variation.

Mid-Pleistocene divergence of Cuban and North American ivory-billed woodpeckers.

We used ancient DNA analysis of seven museum specimens of the endangered North American ivory-billed woodpecker (Campephilus principalis) and three specimens of the species from Cuba to document their degree of differentiation and their relationships to other Campephilus woodpeckers. Analysis of these mtDNA sequences reveals that the Cuban and North American ivory bills, along with the imperial woodpecker (Campephilus imperialis) of Mexico, are a monophyletic group and are roughly equidistant genetically, suggesting each lineage may be a separate species. Application of both internal and external rate calibrations indicates that the three lineages split more than one million years ago, in the Mid-Pleistocene. We thus can exclude the hypothesis that Native Americans introduced North American ivory-billed woodpeckers to Cuba. Our sequences of all three woodpeckers also provide an important DNA barcoding resource for identification of non-invasive samples or remains of these critically endangered and charismatic woodpeckers.