Habitat Loss Does Not Always Entail Negative Genetic Consequences

Although habitat loss has large, consistently negative effects on biodiversity, its genetic consequences are not yet fully understood. This is because measuring the genetic consequences of habitat loss requires accounting for major methodological limitations like the confounding effect of habitat fr...

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Main Authors: Carolina S. Carvalho, Éder C. M. Lanes, Amanda R. Silva, Cecilio F. Caldeira, Nelson Carvalho-Filho, Markus Gastauer, Vera L. Imperatriz-Fonseca, Wilson Nascimento Júnior, Guilherme Oliveira, José O. Siqueira, Pedro L. Viana, Rodolfo Jaffé
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-11-01
Series:Frontiers in Genetics
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fgene.2019.01101/full
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author Carolina S. Carvalho
Éder C. M. Lanes
Amanda R. Silva
Amanda R. Silva
Cecilio F. Caldeira
Nelson Carvalho-Filho
Markus Gastauer
Vera L. Imperatriz-Fonseca
Wilson Nascimento Júnior
Guilherme Oliveira
José O. Siqueira
Pedro L. Viana
Rodolfo Jaffé
Rodolfo Jaffé
author_facet Carolina S. Carvalho
Éder C. M. Lanes
Amanda R. Silva
Amanda R. Silva
Cecilio F. Caldeira
Nelson Carvalho-Filho
Markus Gastauer
Vera L. Imperatriz-Fonseca
Wilson Nascimento Júnior
Guilherme Oliveira
José O. Siqueira
Pedro L. Viana
Rodolfo Jaffé
Rodolfo Jaffé
author_sort Carolina S. Carvalho
collection DOAJ
description Although habitat loss has large, consistently negative effects on biodiversity, its genetic consequences are not yet fully understood. This is because measuring the genetic consequences of habitat loss requires accounting for major methodological limitations like the confounding effect of habitat fragmentation, historical processes underpinning genetic differentiation, time-lags between the onset of disturbances and genetic outcomes, and the need for large numbers of samples, genetic markers, and replicated landscapes to ensure sufficient statistical power. In this paper we overcame all these challenges to assess the genetic consequences of extreme habitat loss driven by mining in two herbs endemic to Amazonian savannas. Relying on genotyping-by-sequencing of hundreds of individuals collected across two mining landscapes, we identified thousands of neutral and independent single-nucleotide polymorphisms (SNPs) in each species and used these to evaluate population structure, genetic diversity, and gene flow. Since open-pit mining in our study region rarely involves habitat fragmentation, we were able to assess the independent effect of habitat loss. We also accounted for the underlying population structure when assessing landscape effects on genetic diversity and gene flow, examined the sensitivity of our analyses to the resolution of spatial data, and used annual species and cross-year analyses to minimize and quantify possible time-lag effects. We found that both species are remarkably resilient, as genetic diversity and gene flow patterns were unaffected by habitat loss. Whereas historical habitat amount was found to influence inbreeding; heterozygosity and inbreeding were not affected by habitat loss in either species, and gene flow was mainly influenced by geographic distance, pre-mining land cover, and local climate. Our study demonstrates that it is not possible to generalize about the genetic consequences of habitat loss, and implies that future conservation efforts need to consider species-specific genetic information.
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spelling doaj.art-c72f07c650484c85831385e8e59106f82022-12-22T01:44:25ZengFrontiers Media S.A.Frontiers in Genetics1664-80212019-11-011010.3389/fgene.2019.01101455095Habitat Loss Does Not Always Entail Negative Genetic ConsequencesCarolina S. Carvalho0Éder C. M. Lanes1Amanda R. Silva2Amanda R. Silva3Cecilio F. Caldeira4Nelson Carvalho-Filho5Markus Gastauer6Vera L. Imperatriz-Fonseca7Wilson Nascimento Júnior8Guilherme Oliveira9José O. Siqueira10Pedro L. Viana11Rodolfo Jaffé12Rodolfo Jaffé13Instituto Tecnológico Vale, Belém, BrazilInstituto Tecnológico Vale, Belém, BrazilInstituto Tecnológico Vale, Belém, BrazilDepartamento de Botânica, Museu Paraense Emílio Goeldi, Belém, BrazilInstituto Tecnológico Vale, Belém, BrazilInstituto Tecnológico Vale, Belém, BrazilInstituto Tecnológico Vale, Belém, BrazilInstituto Tecnológico Vale, Belém, BrazilInstituto Tecnológico Vale, Belém, BrazilInstituto Tecnológico Vale, Belém, BrazilInstituto Tecnológico Vale, Belém, BrazilDepartamento de Botânica, Museu Paraense Emílio Goeldi, Belém, BrazilInstituto Tecnológico Vale, Belém, BrazilDepartamento de Ecologia, Universidade de São Paulo, São Paulo, BrazilAlthough habitat loss has large, consistently negative effects on biodiversity, its genetic consequences are not yet fully understood. This is because measuring the genetic consequences of habitat loss requires accounting for major methodological limitations like the confounding effect of habitat fragmentation, historical processes underpinning genetic differentiation, time-lags between the onset of disturbances and genetic outcomes, and the need for large numbers of samples, genetic markers, and replicated landscapes to ensure sufficient statistical power. In this paper we overcame all these challenges to assess the genetic consequences of extreme habitat loss driven by mining in two herbs endemic to Amazonian savannas. Relying on genotyping-by-sequencing of hundreds of individuals collected across two mining landscapes, we identified thousands of neutral and independent single-nucleotide polymorphisms (SNPs) in each species and used these to evaluate population structure, genetic diversity, and gene flow. Since open-pit mining in our study region rarely involves habitat fragmentation, we were able to assess the independent effect of habitat loss. We also accounted for the underlying population structure when assessing landscape effects on genetic diversity and gene flow, examined the sensitivity of our analyses to the resolution of spatial data, and used annual species and cross-year analyses to minimize and quantify possible time-lag effects. We found that both species are remarkably resilient, as genetic diversity and gene flow patterns were unaffected by habitat loss. Whereas historical habitat amount was found to influence inbreeding; heterozygosity and inbreeding were not affected by habitat loss in either species, and gene flow was mainly influenced by geographic distance, pre-mining land cover, and local climate. Our study demonstrates that it is not possible to generalize about the genetic consequences of habitat loss, and implies that future conservation efforts need to consider species-specific genetic information.https://www.frontiersin.org/article/10.3389/fgene.2019.01101/fullgene flowgenetic diversityisolation by resistancelandscape genomicsopen-pit miningRAD sequencing
spellingShingle Carolina S. Carvalho
Éder C. M. Lanes
Amanda R. Silva
Amanda R. Silva
Cecilio F. Caldeira
Nelson Carvalho-Filho
Markus Gastauer
Vera L. Imperatriz-Fonseca
Wilson Nascimento Júnior
Guilherme Oliveira
José O. Siqueira
Pedro L. Viana
Rodolfo Jaffé
Rodolfo Jaffé
Habitat Loss Does Not Always Entail Negative Genetic Consequences
Frontiers in Genetics
gene flow
genetic diversity
isolation by resistance
landscape genomics
open-pit mining
RAD sequencing
title Habitat Loss Does Not Always Entail Negative Genetic Consequences
title_full Habitat Loss Does Not Always Entail Negative Genetic Consequences
title_fullStr Habitat Loss Does Not Always Entail Negative Genetic Consequences
title_full_unstemmed Habitat Loss Does Not Always Entail Negative Genetic Consequences
title_short Habitat Loss Does Not Always Entail Negative Genetic Consequences
title_sort habitat loss does not always entail negative genetic consequences
topic gene flow
genetic diversity
isolation by resistance
landscape genomics
open-pit mining
RAD sequencing
url https://www.frontiersin.org/article/10.3389/fgene.2019.01101/full
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