Climate change outpaces adaptive potential via hybridization in nesting female Saltmarsh and Nelson’s Sparrows

Ornithology, 2023, 140, 1–15 https://doi.org/10.1093/ornithology/ukad037 Advance access publication 5 August 2023 Research Article Climate change outpaces adaptive potential via hybridization in nesting female Saltmarsh and Nelson’s Sparrows Logan M. Maxwell,1 Jennifer Walsh,2, Brian J. Olsen,3 and Adrienne I. Kovach1,*, Department of Natural Resources and the Environment, University of New Hampshire, Durham, New Hampshire, USA Fuller Evolutionary Biology Program, Cornell Lab of Ornithology, Ithaca, New York, USA 3 School of Biology and Ecology, University of Maine, Orono, Maine, USA 1 2 ABSTRACT Hybridization and introgression can promote adaptive potential and evolutionary resilience in response to increased pressures of climate change; they can also disrupt local adaptation and lead to outbreeding depression. We investigated female fitness consequences of hybridization in two sister species that are endemic to a threatened tidal marsh ecosystem: Saltmarsh (Ammospiza caudacutus) and Nelson’s (Ammospiza nelsoni) sparrows. We found increasing nest flooding rates due to rising sea levels are outpacing potential adaptive benefits of hybridization due to very low overall nesting success in both the Nelson’s and Saltmarsh sparrows. In the center of the hybrid zone across two years, we determined the success of 201 nests of 104 pure and admixed Saltmarsh and Nelson’s Sparrow females, genotyped using a panel of single nucleotide polymorphisms (SNPs) from double digest restriction-site associated DNA (ddRAD) sequencing. We evaluated 5 metrics of female fitness and modeled nesting success in relation to genotypic, environmental, and nesting characteristics. We found differential fitness among Saltmarsh, Nelson’s, and hybrid females, such that birds with predominantly Saltmarsh Sparrow alleles had higher reproductive success than birds with predominantly Nelson’s Sparrows alleles, and hybrids were intermediate. Fledging success increased with two known tidal marsh nesting adaptations: nest height and nesting synchrony with tidal cycles. We found a positive relationship between hybrid index and fitness in daily nest survival in 2016, but not in 2017, likely due to differing levels of precipitation and nest flooding between years. The strongest and most consistent predictors of daily nest survival were nesting synchrony with lunar tidal flooding cycles and daily maximum tide height. Fitness patterns suggest that there may be an adaptive benefit of interspecific geneflow for the Nelson’s Sparrow at the detriment of the Saltmarsh Sparrow; however, flooding rates are so high in many years they mask any fitness differences between the species, and all females had poor nesting success, regardless of genetic makeup. Keywords: adaptive potential, climate change, fitness, hybridization, Nelson’s Sparrow, nest success, Saltmarsh Sparrow, sea-level rise How to Cite Maxwell, L. M., J. Walsh, B. J. Olsen, and A. I. Kovach (2023). Climate change outpaces adaptive potential via hybridization in nesting female Saltmarsh and Nelson’s sparrows. Ornithology 140:ukad037. LAY SUMMARY • This study explores female fitness consequences of hybridization between Saltmarsh and Nelson’s Sparrows. • We evaluated 5 metrics of female fitness, and modeled nesting success in relation to genotype, environment, and nesting characteristics. • We found differential fitness among Saltmarsh, Nelson’s, and hybrid females, such that birds with more Saltmarsh Sparrow alleles had higher reproductive success than birds with predominantly Nelson’s Sparrow alleles, and hybrids had intermediate success. • The most consistent predictors of nest survival and fledging success were daily maximum tide height and female nesting adaptations that mitigate the risk of nest flooding. • High rates of nest flooding due to rising sea levels may be masking species-specific effects and fitness consequences of hybridization due to very low overall nesting success in both species. El cambio climático supera el potencial adaptativo vía hibridación en hembras nidificantes de Ammospiza caudacutus y A. nelsoni RESUMEN La hibridación y la introgresión pueden promover el potencial adaptativo y la resiliencia evolutiva en respuesta a las crecientes presiones del cambio climático; también pueden interrumpir la adaptación local y llevar a depresión híbrida. Investigamos las consecuencias de la Submission Date: March 17, 2023. Editorial Acceptance Date: July 10, 2023 © American Ornithological Society 2023. Published by Oxford University Press for the American Ornithological Society. This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License ((https://creativecommons.org/ licenses/by/4.0/)), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact Corresponding author: * 2 Reproductive success in hybridizing Saltmarsh and Nelson’s Sparrows L. M. Maxwell et al. INTRODUCTION Assessing the fitness and adaptive potential of organisms in vulnerable natural systems is integral for prioritizing conservation actions, particularly in the face of environmental change. Increasingly, wild populations must respond to the combined effects of climate change and anthropogenic modifications of the landscape (i.e., habitat loss, degradation, and fragmentation). To conserve species in the face of rapid environmental change, understanding and assessing their capacity to cope with or respond to these changes (adaptive capacity) is a current research priority, especially for specialist species and ecosystems most vulnerable to climate change (Nicotra et al. 2015). The ability to respond to these rapid changes relies on a combination of mechanisms at both short- and long-term scales (Aitken et al. 2008). Plasticity may allow for rapid, short-term responses to the environment; however, adaptive or evolutionary responses are needed to allow for genetic and resulting phenotypic changes to deal with long-term challenges, such as those imposed by climate change (Savolainen et al. 2007, Aitken et al. 2008, Franks et al. 2013). One potential source of evolutionary resilience (Hamilton and Miller 2015) in light of climate change is inter-specific hybridization and resulting genetic introgression. Recombination of genetic variation due to hybridization may allow for rapid evolution in response to changing selective pressure (Hamilton and Miller 2015). Natural hybridization can augment genetic diversity by extending a species gene-pool, thereby releasing populations from their adaptive constraints (Carlson et al. 2014, Taylor et al. 2015) and allowing for greater adaptive capacity and resilience in response to new environments (Hamilton and Miller 2015, Lewontin and Birch 1966). Indeed, adaptive introgression has been seen in a diversity of hybridizing taxa, including both plants and animals (Lexer et (...truncated)