Abstract

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.

Highlights

  • In spite of ample evidence showing that habitat loss has large, consistently negative effects on biodiversity (Fahrig, 2003), very few studies have assessed the consequences of habitat amount on genetic variation (DiLeo and Wagner, 2016; Monteiro et al, 2019)

  • We identified a total of 10,016 single-nucleotide polymorphisms (SNPs) in B. carajensis and 20,464 SNPs in M. carajensis, but after filtering these for missing data, quality, depth, linkage disequilibrium, deviations from the Hardy-Wenberg Equilibrium, and FST outlier loci, we obtained sets of neutral and independent markers containing 1,411 and 6,052 loci for each species, respectively

  • Cluster-level heterozygosity was slightly higher in B. carajensis than in M. carajensis, and significant albeit low inbreeding was found in one genetic cluster of each species (Figure 2)

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Summary

Introduction

In spite of ample evidence showing that habitat loss has large, consistently negative effects on biodiversity (Fahrig, 2003), very few studies have assessed the consequences of habitat amount on genetic variation (DiLeo and Wagner, 2016; Monteiro et al, 2019). Habitat loss can potentially impact the demographics of natural populations, reducing population size, gene flow, and genetic diversity, and thereby increasing inbreeding and extinction risk (Allendorf et al, 2013). Understanding the genetic consequences of habitat loss is essential to safeguard biological diversity and fulfill Aichi Biodiversity Targets and Sustainable Development Goals (Tittensor et al, 2014). Important limitations constrain the quantification of habitat amount effects on genetic variation. Failure in overcoming any of these limitations may hide important detrimental effects to the maintenance of genetic variability, or reveal spurious patterns unrelated to habitat loss

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