Genomic Consequences of Altered Flood Regimes: Gene Flow and Adaptation in a Threatened Floodplain Plant

Abstract

Floodplains are highly dynamic ecotones where species persistence depends on synchrony between natural flow regimes and life-history. Artificial river engineering has profoundly altered these systems by reducing the frequency and magnitude of spring floods while increasing the unpredictability of flood timing and intensity during summer. These hydrological changes have disrupted historical patterns of dispersal, growth, reproduction, and competitive success among floodplain specialists. Effective conservation in these ecosystems therefore requires understanding how human-altered flow regimes have reshaped floodplain specialists' demography, genetic diversity, genetic connectivity, functional variation, and adaptive potential. Here, we address this challenge in Boltonia decurrens, a federally threatened floodplain plant endemic to the Illinois River Valley, by integrating a chromosome-scale reference genome, whole-genome resequencing, and common-garden adaptive trait measurements from 424 individuals across 17 populations. Demographic analyses revealed a severe recent bottleneck and a subsequent rebound. Population structure was clinal with downstream-dominant gene flow, indicating that regional population connectivity predominates over longer-distance gene flow. A subset of populations showed elevated genetic isolation with increased inbreeding and homozygous deleterious burden, revealing a genomic cost of disrupted floodplain connectivity. Common-garden observations and GWAS showed extensive within-population phenotypic and genetic variation in flowering time, flowering stem height, and year of first flowering (1st vs. 2nd year), which are hypothesized to buffer populations and to be selectively maintained under human-altered flow regimes. Finally, landscape-genomic approaches detected a divergent haplotype block separating northern and southern populations, suggesting that adaptive divergence can persist even in a system shaped by recurrent disturbance and ongoing gene flow.