Species confined to naturally fragmented habitats may exhibit intrinsic population complexity which may challenge interpretations of species response to anthropogenic landscape transformation. In South Africa, where native forests are naturally fragmented, forest‐dependent birds have undergone range declines since 1992, most notably among insectivores. These insectivores appear sensitive to the quality of natural matrix habitats, and it is unknown whether transformation of the landscape matrix has disrupted gene flow in these species. We undertook a landscape genetics study of four forest‐dependent insectivorous songbirds across southeast South Africa. Microsatellite data were used to conduct a priori optimization of landscape resistance surfaces (land cover, rivers and dams, and elevation) using cost‐distances along least‐cost pathway (LCP), and resistance distances (IBR). We detected pronounced declines in effective population sizes over the past two centuries for the endemic forest specialist Cossypha dichroa and Batis capensis, alongside recent gene flow disruption in B. capensis, C. dichroa and Pogonocichla stellata. Landscape resistance modelling showed both native forest and dense thicket configuration facilitates gene flow in P. stellata, B. capensis and C. dichroa. Facultative dispersal of P. stellata through dense thicket likely aided resilience against historic landscape transformation, whereas combined forest‐thicket degradation adversely affected the forest generalist B. capensis. By contrast, Phylloscopus ruficapilla appears least reliant upon landscape features to maintain gene flow and was least impacted by anthropogenic landscape transformation. Collectively, gene flow in all four species is improved at lower elevations, along river valleys, and riparian corridors— where native forest and dense thicket better persist. Consistent outperformance of LCP over IBR land‐cover models for P. stellata, B. capensis and C. dichroa demonstrates the benefits of wildlife corridors for South African forest‐dependent bird conservation, to ameliorate the extinction debts from past and present anthropogenic forest exploitation.

Blood tissues samples of 114 Batis capensis, 94 Cossypha dichroa, 92 Phylloscopus ruficapilla, and 200 Pogonicichla stellata were collected from forests across southeast South Africa. From these samples, genomic DNA was extracted using a Nucleospin Tissue DNA extraction kit (Macherey‐Nagel). For each species, we screened a separate microsatellite library available from past literature (9–29 loci per species; 55 loci total) and obtained for each species a unique combination of eight informative loci. We randomized within‐species samples prior to amplification to minimize false‐positive discovery from downstream analyses. Microsatellite alleles were genotyped on an ABI377xlsequencer (CAF, Stellenbosch), and scored against LIZ 500© internal size marker, using three positive control individuals per species for each marker to verify scoring accuracy. We screened all microsatellite loci for amplification errors (large allele dropout, stuttering and null alleles), and assessed forest subpopulation‐level deviations from expectations of Hardy–Weinberg equilibrium and linkage disequilibrium adjusting significance values using a Benjamini–Hochberg correction to control for false discovery rate. 

Usage: population genetics, landscape genetics, demographic analysis.

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