Genomic Consequences of Biological Invasions: Systematic Insights from Anopheles stephensi and Comparative Analyses Across Taxa

Abstract

Biological invasions often begin with small founding populations that reduce population size, increase homozygosity, and can trigger large-scale ecological change. Yet many invaders still persist and spread in new areas despite the evolutionary costs expected from establishing small, isolated populations. This dissertation links an applied, species-level analysis of the invasive malaria vector in Africa, Anopheles stephensi, with cross-taxon genomic analyses to understand how ecological flexibility and genomic mechanisms jointly shape invasion outcomes. First, a range-wide synthesis of An. stephensi bionomics reveals flexible larval habitat use, urban adaptation, and variable biting and resting behavior. In invaded ranges, these shifts alter surveillance yields and intervention efficacy relative to native settings, outlining the ecological plasticity may facilitate establishment in new landscapes. Building from this, the second chapter generalized genomic consequences of invasion across eleven taxa using standardized pipelines to quantify nucleotide diversity, heterozygosity, and runs of homozygosity (ROH). Genomes sampled from the invasive range showed reduced nucleotide diversity on average, although several invasive species retained or exceeded nucleotide diversity compared to their native counterparts. Runs of homozygosity varied across species, with some genomes from the introduced range containing long autozygous segments while others maintained short or sparse runs, likely indicating comparatively larger founding sizes or post establishment gene flow. We also found that genetic diversity in introduced populations was often enriched near chromosome ends while central regions remained depleted, and this genome structure contrast was driven more by how introductions occurred than by generation time or years since introduction. Together, these findings show that invasion pathways and recombination landscapes jointly determine whether invasive populations emerge from bottlenecks with genomes that are depleted, resilient, or even enriched for diversity, directly addressing the dissertation goal of explaining why some invaders thrive while others stall. Building on this, the third chapter uses the same eleven species to link genome architecture to an explicit evolutionary consequence: changes in realized recessive genetic load, quantified as the number and placement of homozygous deleterious variants that influence long term fitness and persistence. Genomes sampled from the invaded range carried 36% fewer homozygous high-impact genetic variants than the native range sampled genomes. This reduction was driven by variants found outside runs of homozygosity, indicating that purging primarily removed deleterious alleles from non-autozygous regions. Differences across variant impact classes revealed that purging signals were strongest at low and moderate severity SNPs, suggesting that drift and selection during invasion act primarily on numerous mildly deleterious alleles rather than on rare, strongly deleterious ones. Taken together, these chapters link ecology and genome dynamics: the species-level An. stephensi case study illustrates the conditions that enable establishment in urban environments, while the cross-taxon comparative and functional genomics explain why establishment can persist despite bottlenecks, since propagule pressure and recent admixture reshape ROH patterns and reduce realized recessive load, thereby sustaining fitness in novel settings. Overall, this work shows that invasion success depends less on time since introduction than on the match between ecological opportunity, introduction pathways, and genome architecture. This integration frames invasion genomics as the interaction between ecological opportunity and genome architecture and supports practice by pairing bionomics-aware surveillance and control with genomic monitoring of diversity, ROH placement, and load to anticipate spread potential and tailor interventions.