Geographically consistent hybridization dynamics between the Black-crested and Tufted titmouse with evidence of hybrid zone expansion

Ornithology, 2023, 140, 1–13 https://doi.org/10.1093/ornithology/ukad014 Advance access publication 8 April 2023 Research Article Geographically consistent hybridization dynamics between the Black-crested and Tufted titmouse with evidence of hybrid zone expansion Claire M. Curry,2,a,# Michael A. Patten,3 Jason T. Weir,4,5,6 and Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, Colorado, USA Department of University Libraries, Ecology and Evolutionary Biology Program and Oklahoma Biological Survey, University of Oklahoma, Norman, Oklahoma, USA 3 Department of Ecology Research Group, Faculty of Biosciences and Aquaculture, Nord University, Steinkjer, Norway 4 Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Ontario, Canada 5 Department of Biological Sciences, University of Toronto Scarborough, Toronto, Ontario, Canada 6 Department of Ornithology, Royal Ontario Museum, Toronto, Ontario, Canada a Current address: University Libraries, University of Oklahoma, Norman, Oklahoma, USA 1 2 #These authors contributed equally to the paper. * Corresponding author: ABSTRACT We studied hybridization between the Black-crested and Tufted titmouse across two geographically distinct transects that differ in the timing of secondary contact by hundreds to thousands of years. We found that hybridization patterns correspond to localized hybrid swarms and that the titmouse hybrid zone is likely slowly expanding over time, a product of short post-natal dispersal distances coupled with weak or absent selection against admixture. We show the southern part of the hybrid zone located in Texas is four times wider than the northern region of hybridization in Oklahoma, which is likely due to geographic differences in hybrid zone age. Despite differences in width, most individuals in both transects are advanced-generation hybrids and backcrosses, suggesting geographically consistent hybridization dynamics. We documented a strong correlation between genotypes and plumage index, suggesting that hybridization has not yet resulted in the decoupling of plumage and genome-wide ancestry as observed in some other avian hybrid zones. Although our results suggest the ongoing expansion of the hybrid zone, the rate of expansion appears to be slow, on the scale of tens of meters a year, and it will likely take hundreds of thousands to millions of years before homogenization of the parental populations. While we did not find support for partial reproductive isolation in the hybrid zone itself, there is the possibility that ecological or sexual selection limits introgression into allopatric regions. Broadly, the results of our study highlight the value of multiple, geographically distant, transects across a hybrid zone for assessing the evolutionary dynamics of hybridizing lineages. Keywords: Black-crested titmouse, hybridization, hybrid swarm, introgression, reproductive isolation, Tufted titmouse How to Cite Semenov, G. A., C. M. Curry, M. A. Patten, J. T. Weir, and S. A. Taylor (2023). Geographically consistent hybridization dynamics between the Black-crested and Tufted Titmouse with evidence of hybrid zone expansion. Ornithology 140:ukad014. LAY SUMMARY • We studied hybridization patterns between Black-crested and Tufted titmice in two areas of their contact zone that differ in the age of onset of hybridization by hundreds or thousands of years. • We show that northern (younger) parts of the hybrid zone have a genetic transition four times narrower than the southern (older) region, which plausibly reflects the differences in the hybrid zone age or is a result of differences in the breadth of the ecotone between titmouse habitats in the north and south. • Our results suggest that the Black-crested and Tufted titmouse hybrid zone might be in the process of slowly expanding following selectively neutral hybridization dynamics, although we cannot completely rule out a possible role of ecological or sexual selection in limiting gene flow outside of the hybrid zone. Submission Date: July 15, 2022. Editorial Acceptance Date: March 27, 2023 Copyright © American Ornithological Society 2023. All rights reserved. For permissions, e-mail: . Georgy A. Semenov,1,#,*, Scott A. Taylor1 2 Hybridization between Black-crested and Tufted titmouse G. A. Semenov et al. Dinámicas de hibridación geográficamente consistentes entre Baeolophus atricristatus y B. bicolor con evidencia de expansión de la zona híbrida RESUMEN INTRODUCTION Hybrid zones continue to advance our understanding of the mechanisms promoting or reversing reproductive isolation between nascent species and, on a broader scale, the origin of biological diversification (Hewitt 1988, Payseur and Rieseberg 2016, Taylor and Larson 2019). In particular, the dynamic nature of hybridization provides an opportunity to use phenotypic and genetic patterns to assess the strength of reproductive barriers and to evaluate the evolutionary trajectory of hybridizing taxa. Moreover, a combination of selection on certain genomic regions coupled with introgression throughout the rest of the genome—which sometimes results in the strong decoupling of phenotypic variation from genome-wide genetic ancestry—has enabled a growing collection of studies to successfully dissect the genetic basis of traits involved in reproductive isolation and speciation (e.g., Poelstra et al. 2014, Toews et al. 2016, Semenov et al. 2021). Many hybrid zones follow the tension hybrid zone model (Slatkin 1973, Barton and Hewitt 1985), where zone width is determined by the interplay between the dispersal of parental genotypes into the region of hybridization and selection against admixed genotypes that are maladaptive. Under the tension zone model, the hybrid zone width will remain narrower than expected under a scenario of unrestricted hybridization and neutral diffusion, and a comparison of observed and expected hybrid zone widths can provide insight into the action of selection. Further, the interaction between dispersal and selection can produce an array of patterns informative about hybrid zone dynamics. For example, strong selection against hybridization (e.g., due to positive assortative mating) or hybrids (e.g., due to postzygotic selection) coupled with ongoing dispersal of parentals will result in a bimodal distribution (i.e., two modes corresponding to each parental genotype) of genetic ancestries in the hybrid zone center (Gay et al. 2008). With some level of hybridization and introgression, as well as selection against hybrids and backcrosses, the distribution of genetic ancestries will appear trimodal (two modes for parental genotypes and one for the hybrids; Gay et al. 2008). In such scenarios, sample variance in genotypes across the hybrid zone will increase towards the hybrid zone center (Gay et al. 2008, Semenov et al. 2017). Conversely, small dispersal d istances coupled with weak (or no) selection will produce a hybri (...truncated)