What makes a successful invader? Population genomics and adaptation to novel environments in the invasive Japanese white-eye (Zosterops japonicus)

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2021

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Abstract

Invasive species face many obstacles when colonizing new habitats. Yet, many overcome these hurdles and successfully establish populations. Therefore, understanding how invasive species cope with novel stressors while colonizing new environments is a fundamental goal of evolutionary biology. Additionally, broadening our understanding of how birds adapt to novel environments can help us predict how species will respond to habitat degradation and stressors resulting from climate change in the future. Here, we focus on the Japanese white-eye (Zosterops japonicus), an East Asian bird that was introduced into Hawaii in the early 1900s and is now the most abundant land bird in the archipelago. First, we sequenced and assembled a high-quality Z. japonicus genome and compared genome annotation pipelines. We found that AUGUSTUS was more conservative with gene predictions when compared to BRAKER2, but the final number of annotated gene models was similar between the two workflows. Additionally, we found that while adding more data did not significantly change the number of annotated genes using AUGUSTUS, using BRAKER2 the number increased substantially. Next, we compared whole genomes of Z. japonicus individuals from both their native and introduced ranges to characterize genetic diversity and population history and divergence and to identify genes potentially under selection between the two populations. We saw evidence of mixed ancestry in the introduced population, supported by drastically different demographic histories in Hawaii. This suggests that admixture could have contributed to increased genetic diversity in the introduced population and therefore to overall invasion success. Lastly, we conducted one-, three-, and six-week one-way transplants of individuals from near sea level to 2,790m, with individuals kept at sea level as controls, and later a six-week reciprocal transplant from high to low elevation and vice versa. We assessed morphological and physiological traits as well as gene expression using RNA-seq on heart and lung tissues. We found strong evidence for phenotypic plasticity in hematological and cardiac response to hypoxia and cold stress and some evidence of maladaptive plasticity in pulmonary circulation. We identified two genes potentially under divergent selection in the high elevation population that could be indicative of early-stage genotypic specialization in response to hypoxia and cold stress. Our results suggest that the population of Z. japonicus on Mauna Kea is able to persist at high elevation because of ancestral plasticity, which also could have contributed to its remarkable success as an invasive species.

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