Hybrid Speciation in Amazonian Birds

Hybridization can erode diversity, but may also contribute importantly to the speciation process. Our lab is actively studying various populations of hybrid origin to better understand both the creative and destructive roles played by hybridization. One of our labs recent discoveries was that the highly range restricted and rarely observed Golden-crowned Manakin appears to be a hybrid species, with demographic modelling suggesting it originated roughly 180 thousand years ago through hybridization between the spectacularly coloured Snow-capped and Opal-crowned Manakins (read.here). This would be the first avian hybrid species reported from the rainforests of the Amazon and one of the few hybrid species of animal in which the phenotype is not intermediate between the parental species. Ongoing research in the lab involves analyses of whole genome sequences to characterize the differentiation of these manakins. Lab PhD student Else Mikkelsen has also used whole-genome sequencing to mitogenomic capture and nuclear introgression involving the Great Skua and Pomarine Jaeger (Systematic Biology, in press)

The Genomics of Speciation

A recent focus of the lab is on the genomics of speciation, and how the genetic architecture of reproductive isolation varies between birds living in the rainforests of the Amazon versus the boreal forests of Canada. Our past work has shown that closely related bird species in the tropics continue to form hybrid zones for up to four million years following divergence (see figure on left), while the oldest hybrid zones at boreal latitudes are less than 1.5 million years old (read.here). The older age of hybridizing species in the tropics suggests that tropical species are accumulating reproductive isolation more slowly there, and thus taking a longer time to complete

the process of speciation. Our research also demonstrates that many species pairs believed to be separated by major Amazonian rivers, come into geographic contact in headwater regions where they invariably form hybrid zones (read.here). Lab members are utilizing genome-wide and whole genome datasets to investigate the genetic architecture of reproductive isolation in tropical and temperate regions. The lab has recently sequenced, assembled, and annotated 38 de novo reference genomes and our projects now use a mix of genome-reduction methods and whole genome resequencing.

Phylogenetic estimates of speciation and extinction rates

Are speciation rates fastest in the tropics, and can they explain the high species richness there? Using phylogenetic data we showed that rates of speciation have been much faster at high latitudes, and slower in the tropics over the past few million years. In contrast, extinction rates were very slow in the tropics, and might explain how the tropics have been able to accumulate such high levels of species richness (read here). Recent research by former Ph.D. student Dr. Paola Pulido-Santacruz extended this work across the entire bird phylogeny. Her work suggests that extinction rates are consistently lower in geographic regions with low species richness across many replicate orders of birds, while speciation rates showed no consistent pattern with latitude across replicate clades (read here). Together, these studies suggest that low tropical extinction could be the key historical driver behind the latituidnal diversity gradient.

Latitudinal gradients in trait evolution

We investigate whether rates of evolution vary across latitudinal and ecological gradients in traits (song, colour, morphometrics and climatic niche) important for speciation and ecological differentiation. A key focus has been on rates of evolution in the courtship songs used by birds to attract mates. Our results demonstrate faster evolution of bird song (Weir & Wheatcroft 2011, Proc. Roy B; Weir et al. 2012 Evolution. Former MSc student Adam Lawson demonstrated a much faster rate of climatic niche evolution at high latitudes, suggesting that divergent selection pressures are stronger towards the poles (Lawson & Weir 2014, Ecology Letters) while PhD student Vanessa Luzuriaga-Aveiga has demonstrated that increased elevational differentiation results in increased rates of song and morphometric trait evolution across the Amazon and eastern Andean slopes (Luzuriaga-Aveiga & Weir 2019, Ecology Letters). PhD student Sean Anderson has developed new models of trait evolution (and a new R package) that quantify the degree of divergent adaptation (Anderson & Weir 2020, Am. Nat.) and more recently that distinguish between character displacement,

ecological sorting or time as explanations for greater trait divergence in sympatric versus allopatric sister species pairs. His key finding is that an overwhelming signature of character displacement characterizes continental faunas, with the effect strongest in the tropics (Anderson & Weir 2021, PNAS). Compiling one of the largest comparative datasets involving morphometric traits yet examined, Sean applied our newest trait evolution models which estimate the proportion of species pairs evolving under divergent selection during the critical, initial allopatric phase of speciation to be only about 10%. These results argue against ecological speciation via divergent selection as a key driver of most speciation events and instead suggests that niche conservatism or parallel ecological selection may be the dominant drivers (Anderson & Weir 2022, Science).

Comparative Phylogeography and Biogeography

An ongoing focus of the lab is to utilize comparative approaches across many species to address key biogeographic questions such as the role of ice sheets in driving allopatric speciation in boreal birds (read.here) and New Zealand kiwi (read here), the role of climate change in driving diversification of lowland and highland birds of the Neotropics (read here), and the role of landbridge completion in driving the Great American Biotic Interchange between North and South American birds (read here). We are using genome-wide and whole genome datasets to study phylogeographic questions in a variety of other North American and Amazonian species: manakins (Ph.D. student Else Mikkelsen and former student Dr. Alfredo Barrera-Guzman), antbirds (former students Dr. Aurea Cronemberger and Dr. Maya Faccio), tanagers (Ph.D. student Vanessa Luzuriaga), flyctachers (former post doc Dr. Jordan Bemmels), warblers, thrushes (with collaborators Alyssa FitzGerald and Jeremy Kirchmam), titmice (with collaborator Claire Curry), and kiwi (with former post doc Dr. Jordan Bemmels).

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