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Evidence of local adaptation despite strong drift in a Neotropical patchily distributed bromeliad

Abstract

Both genetic drift and divergent selection are predicted to be drivers of population differentiation across patchy habitats, but the extent to which these forces act on natural populations to shape traits is strongly affected by species’ ecological features. In this study, we infer the genomic structure of Pitcairnia lanuginosa, a widespread herbaceous perennial plant with a patchy distribution. We sampled populations in the Brazilian Cerrado and the Central Andean Yungas and discovered and genotyped SNP markers using double-digest restriction-site associated DNA sequencing. In addition, we analyzed ecophysiological traits obtained from a common garden experiment and compared patterns of phenotypic and genetic divergence (PSTFST comparisons) in a subset of populations from the Cerrado. Our results from molecular analyses pointed to extremely low genetic diversity and a remarkable population differentiation, supporting a major role of genetic drift. Approximately 0.3% of genotyped SNPs were flagged as differentiation outliers by at least two distinct methods, and Bayesian generalized linear mixed models revealed a signature of isolation by environment in addition to isolation by distance for high-differentiation outlier SNPs among the Cerrado populations. PSTFST comparisons suggested divergent selection on two ecophysiological traits linked to drought tolerance. We showed that these traits vary among populations, although without any particular macro-spatial pattern, suggesting local adaptation to differences in micro-habitats. Our study shows that selection might be a relevant force, particularly for traits involved in drought stress, even for populations experiencing strong drift, which improves our knowledge on eco-evolutionary processes acting on non-continuously distributed species.

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Fig. 1: Population sampling and genetic structure of Pitcairnia lanuginosa as inferred by INSTRUCT analysis.
Fig. 2: Neighbor-net analysis.
Fig. 3: Candidate SNPs bearing a signal of selection.
Fig. 4: Forest plot comparing means and confidence intervals of PST for 11 phenotypic traits and neutral FST among eight Cerrado populations of Pitcairnia lanuginosa based on 1000 bootstraps.

Data availability

The PyRAD outputs generated from the de novo assembly of RAD-seq data, as well as ecophysiological data collected from the common garden experiment, are available on the Dryad Digital Repository https://doi.org/10.5061/dryad.zpc866t84. Raw reads have been deposited in the NCBI SRA database (BioProject ID: PRJNA723200; BioSample accessions: SRR14279592-SRR14279706).

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Acknowledgements

We thank S. Nazareno, M. Arakaki, and P.H. Egoavil for assisting in sampling and permission procedures, and E. Guichoux for helping in the preparation of ddRAD-seq libraries. We are also grateful to K. Holsinger and two anonymous reviewers for providing helpful comments on the earlier version of the manuscript and to the Genotoul bioinformatics platform Toulouse Midi-Pyrenees (Bioinfo Genotoul) and the Center for Scientific Computing (NCC/GridUNESP) of the São Paulo State University (UNESP) for providing computing and storage resources. This work was supported by Fundação de Apoio à Pesquisa do Estado de São Paulo (FAPESP; 2014/15588-6) and has benefited from the support of a grant from Investissement d’Avenir grants of the ANR (CEBA:ANR-10-LABX-25-01). BSSL and CJNC received scholarships from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES; code 001) and FAPESP (2014/08087-0 and 2016/04396-4). BSSL also received a LabEx COTE mobility grant and a BEPE FAPESP scholarship (2016/20273-0). CPS was funded by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq; 300819/2016-1). Collection and export permits were granted by SISBIO (no. 44062-1), SERFOR (RDG no. 2017-2016), IDEFLOR-Bio/PA (no. 001/15), SEMARH/GO (no. 187/2014) and IEF/MG (no. 081/2014).

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BSSL, CJNC, MH, and CPS conceived the ideas; BSSL, CJNC, LAPH, and CPS sampled the populations; BSSL, VAG, and CB collected molecular data; CJNC measured the ecophysiological traits; BSSL and CJNC analyzed the data; and BSSL, CJNC, MH, and CPS led the writing. All authors read and accepted the final version.

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Correspondence to Bárbara Simões Santos Leal.

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Leal, B.S.S., Chaves, C.J.N., Graciano, V.A. et al. Evidence of local adaptation despite strong drift in a Neotropical patchily distributed bromeliad. Heredity (2021). https://doi.org/10.1038/s41437-021-00442-9

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