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Patterns of Introgression Vary Within an Avian Hybrid Zone Logan M

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Patterns of Introgression Vary Within an Avian Hybrid Zone Logan M Maxwell et al. BMC Ecol Evo (2021) 21:14 BMC Ecology and Evolution https://doi.org/10.1186/s12862-021-01749-1 RESEARCH ARTICLE Open Access Patterns of introgression vary within an avian hybrid zone Logan M. Maxwell1, Jennifer Walsh1,2, Brian J. Olsen3 and Adrienne I. Kovach1* Abstract Background: Exploring hybrid zone dynamics at diferent spatial scales allows for better understanding of local factors that infuence hybrid zone structure. In this study, we tested hypotheses about drivers of introgression at two spatial scales within the Saltmarsh Sparrow (Ammospiza caudacuta) and Nelson’s Sparrow (A. nelsoni) hybrid zone. Specifcally, we evaluated the infuence of neutral demographic processes (relative species abundance), natural selec- tion (exogenous environmental factors and genetic incompatibilities), and sexual selection (assortative mating) in this mosaic hybrid zone. By intensively sampling adults (n 218) and chicks (n 326) at two geographically proxi- mate locations in the center of the hybrid zone, we determined= patterns of introgression= on a fne scale across sites of difering habitat. We made broadscale comparisons of patterns from the center with those of prior studies in the southern edge of the hybrid zone. Results: A panel of fxed SNPs (135) identifed from ddRAD sequencing was used to calculate a hybrid index and determine genotypic composition/admixture level of the populations. Another panel of polymorphic SNPs (589) was used to assign paternity and reconstruct mating pairs to test for sexual selection. On a broad-scale, patterns of introgression were not explained by random mating within marshes. We found high rates of back-crossing and similarly low rates of recent-generation (F1/F2) hybrids in the center and south of the zone. Ofspring genotypic proportions did not meet those expected from random mating within the parental genotypic distribution. Addition- ally, we observed half as many F1/F2 hybrid female adults than nestlings, while respective male groups showed no diference, in support of Haldane’s Rule. The observed proportion of interspecifc mating was lower than expected when accounting for mate availability, indicating assortative mating was limiting widespread hybridization. On a fne spatial scale, we found variation in the relative infuence of neutral and selective forces between inland and coastal habitats, with the smaller, inland marsh infuenced primarily by neutral demographic processes, and the expansive, coastal marsh experiencing higher selective pressures in the form of natural (exogenous and endogenous) and sexual selection. Conclusions: Multiple drivers of introgression, including neutral and selective pressures (exogenous, endogenous, and sexual selection), are structuring this hybrid zone, and their relative infuence is site and context-dependent. Keywords: Ammospiza caudacutus, Ammospiza nelsoni, Hybrid zone, Introgression, Natural selection, Sexual selection, Demographics, Haldane’s rule, Assortative mating, Exogenous selection Background Understanding hybrid zone structure, including spatial patterns of introgression and character variation, can *Correspondence: [email protected] 1 Department of Natural Resources and the Environment, University help infer processes that maintain hybrid zones and pro- of New Hampshire, Durham, NH, USA vide important insights into the nature of species bound- Full list of author information is available at the end of the article aries [1–3]. Spatial variation in hybridization rates and © The Author(s) 2021. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Maxwell et al. BMC Ecol Evo (2021) 21:14 Page 2 of 18 outcomes can reveal correlations between hybrid-zone environmental gradients predict patterns of introgression structure and specifc features of local environmental [13]. conditions as well as local population dynamics [4]. Out- Endogenous selective factors may also play a part in comes of hybridization and introgression can vary based hybrid zone structure, whereby adaptation is on the on numerous factors, including local population demo- genomic level and independent of the external environ- graphics (relative species abundances), exogenous natu- ment [19, 20]. Hybrid individuals may be selected against ral selection (environmental efects on hybrid ftness), due to genetic incompatibilities leading to inviability/ endogenous natural selection (genetic incompatibilities sterility or reduced ftness, and this in turn can contrib- and heterosis), and sexual selection (mate competition ute to maintaining species boundaries [21, 22]. Selection and mating preferences). Identifying the relative infu- against hybrids may also difer between sexes. For exam- ence of these processes in a hybrid zone is important for ple, Haldane’s Rule predicts that the heterogametic sex of understanding spatial variation in introgression and pre- frst-generation hybrids should experience greater reduc- dicting future hybrid zone dynamics. tions in ftness [23, 24]. Tis reduced ftness can result Diferences in rates of hybridization and patterns of from lower fertility or survival, both of which have been introgression due to local demographics and population observed in avian hybrid zones [20, 24]. size have been seen in a variety of taxa, including birds Interspecifc competition and assortative mating have [5–8], and can play a key role in hybrid zone structure. also been shown to infuence patterns of hybridization Hubbs Principle [9] asserts that if population sizes are and introgression across hybrid zones by means of sexual unequal between parental species, hybridization will be selection. Some mating behaviors may promote hybridi- more widespread due to restricted mate choice for the zation and gene fow, while others may inhibit it. One rarer species [10]. Further, when one species is rare rela- species may have a consistent competitive mating advan- tive to the other, hybrid fertilizations may constitute a tage or dominance over the other, regardless of the spe- larger proportion of the total matings of the rarer species, cies identity of the mate, resulting in unidirectional gene and if hybrids backcross diferentially to the common fow and asymmetrical introgression [25, 26]. Alterna- parental taxa, this can lead to genetic assimilation [6, 11]. tively, assortative mating may preserve species bounda- For example, in the Golden-winged (Vermivora chrys- ries and maintain bimodal population structure due to optera)- Blue-winged Warbler (V. pinus) hybrid zone, pre- or post-copulatory processes [27]. rates of introgression vary across sites that difer in rela- In this study, we investigated patterns of introgression tive population size and status of the two species, such and drivers of gene fow at broad and fne spatial scales in that when Golden-winged Warbler populations were at a the Saltmarsh Sparrow (Ammospiza caudacuta) and Nel- minimum, introgression was more prevalent than in pop- son’s Sparrow (A. nelsoni) hybrid zone. Tese two spar- ulations with more equal proportions of the two species row species have restricted breeding habitat along the [7]. However, if parental populations are highly skewed northeastern Atlantic coast of the United States. Nelson’s toward one species, the absolute rate of hybridization Sparrows breed in marshes from the Canadian Maritimes may be limited due to the reduced number of individual to Massachusetts and the Saltmarsh Sparrow’s range interactions between the two species. Tis can be espe- extends from southern Maine to Virginia [28, 29]. Tese cially true in promiscuous mating systems that depend sister species co-inhabit marshes where their ranges on encounter rates, such that members of the rarer spe- overlap, forming a ~ 200 km, linear hybrid zone along the cies may be less likely to fnd mates [12]. New England coast ([30–34]; Fig. 1). Saltmarsh Sparrows Patterns of introgression can also vary substantially are entirely restricted to tidal salt marshes, while Nelson’s across hybrid zones due to variation in hybrid ofspring Sparrows will also breed in brackish, less tidal coastal or parental species ftness in the local environment. marshes, and have been known to inhabit hayfelds and Diferential adaptation along environmental gradients fens [28, 31, 35]. In turn, Saltmarsh Sparrows show a explain patterns of hybridization and introgression in number of adaptations that increase their ftness in fully many systems [5, 13–15]. In particular, habitat prefer- estuarine marshes relative to Nelson’s Sparrows [36, 37]. ence
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