Genetic effects of anthropogenic habitat fragmentation on remnant animal and plant populations: a meta‐analysis

Abstract

Habitat loss and fragmentation are among the biggest threats to biodiversity. Anthropogenic habitat fragmentation leads to small and isolated remnant plant and animal populations. The combination of increased random genetic drift, inbreeding, and reduced gene flow may substantially reduce genetic variation of remnant populations. However, the magnitude of these responses may depend on several poorly understood factors including organism group, habitat type of both the fragment and the surrounding matrix, life-history traits, and time since fragmentation. We compiled data for 83 plant and 52 animal species and conducted a meta-analysis following best practices to evaluate how these factors mediate the effects of anthropogenic habitat fragmentation. We calculated 206 effect sizes as correlations between one of four measures of population-level genetic diversity and fragment area. All analyses were repeated using models of increasing complexity (traditional random-effects models, multilevel models accounting for non-independent data, and multilevel models additionally correcting for phylogenetic relatedness). We confirmed that anthropogenic habitat fragmentation has overall negative effects on genetic diversity of organisms. Our meta-analysis shows, however, that plant species responded in general stronger to fragmentation than animal species and that the largest negative impacts of fragmentation occurred in tropical and temperate forest fragments, surrounded by a non-forest matrix. In contrast, we found only weak responses in non-forest fragments. Genetic diversity measured as mean number of alleles (A) showed the strongest response to fragmentation. Expected heterozygosity (He) and percentage of polymorphic loci (PLP) showed similar but weaker responses. In contrast, our meta-analysis indicated that inbreeding (Fis) was not measurably affected by anthropogenic habitat fragmentation. Additionally, our models revealed that effects on genetic diversity became stronger with age of fragments: We found significant negative responses for fragments older than 50 yr but not for those more recently isolated. Our meta-analyses also showed that currently animals are underrepresented in the literature on genetic effects of anthropogenic fragmentation, as are certain geographical regions and habitat types. We expect that future field studies using state-of-the-art approaches will provide further evidence of negative genetic effects, which may reinforce the here reported patterns, even for groups not yet studied.

No consistent effects of humans on animal genetic diversity worldwide

“…Trends in intraspecific genetic diversity are expected to be scale‐dependent, as are trends in other dimensions of biodiversity like taxonomic, phylogenetic and functional diversity (McGill et al ; Jarzyna & Jetz ; Schlaepfer et al ; Chase et al ). Moreover, human disturbances occurring at different scales may have contrasting effects on genetic diversity.…”

“…As such, understanding the drivers of genetic diversity change worldwide is of great interest to ecologists and conservation biologists (Hughes et al 2008;Pereira et al 2013;Mimura et al 2017;Paz-Vinas et al 2018). Human disturbances, acting as an evolutionary force by modifying rates of extinction and colonisation (Palumbi 2001;Alberti 2015;Thomas 2015;Schlaepfer et al 2018), may be altering the intraspecific genetic diversity of plants and animals around the world-yet no global assessment of temporal trends in genetic diversity has been conducted to date, nor have human impacts on such trends been quantified.…”

Worldwide impacts of humans on animal genetic diversity

“…Understanding the drivers of genetic diversity change worldwide, across taxonomic groups, is of great interest to ecologists and conservation biologists (Hughes et al 2008;Pereira et al 2013;Mimura et al 2017;Paz-Vinas Ivan et al 2018). Humans are now acting as an evolutionary force, modifying rates of extinction and colonization, but also altering the intraspecific genetic diversity of plants and animals around the world (Palumbi 2001;Alberti 2015;Thomas 2015;Schlaepfer et al 2018). To date, no global assessment of temporal trends in genetic diversity has been conducted, nor have human impacts on such trends been quantified.…”

“…Trends in intraspecific genetic diversity are expected to be scale-dependent as are trends in other dimensions of biodiversity (McGill et al 2015;Jarzyna & Jetz 2018;Schlaepfer et al 2018). Human disturbances occur at different scales (e.g., habitat loss and fragmentation) but the impacts on genetic diversity should be strongest at the scales that impact the size and fitness of individual populations and migration among them within metapopulations.…”

Genetic diversity and connectivity in fragmented populations of Rhinanthus minor in two regions with contrasting land-use

“…Habitat fragmentation is detrimental to genetic diversity as well as species diversity (Kahilainen et al 2014;Schlaepfer et al 2018). An increased understanding of genetic variation and connectivity in species found in habitats of high nature value is key to the development of conservation strategies for small and isolated populations (Picó and van Groenendael 2007;Mijangos et al 2015).…”