Apomixis imposes evolutionary costs by reducing recombination efficiency and disrupting segregation

Sexual reproduction facilitates the purging of deleterious mutations via recombination. Apomixis, defined by asexual seed formation, involves suppressed meiosis, thereby reducing the efficacy of purifying selection. However, the evolutionary consequences of apomixis remain poorly understood. In this study, we used wild citrus (Citrus hindsii), which has both sexual and apomictic (adventitious embryony) lineages, as a diploid genetic system (2n = 2x = 18). We performed a cross between a sexual and an apomictic individual (pollen donor), generated haplotype-resolved genome assemblies for the two parents, and deep-sequenced 226 progeny. These data were integrated into a graph pangenome to characterize the meiotic recombination landscape. The apomictic lineage harbors 1.28-fold more heterozygous structural variations, which may locally suppress crossovers. Furthermore, apomictic recombination efficiency is reduced by 24.2% relative to the sexual lineage. Crucially, the contribution of male function through outcrossing exposes a substantial recessive genetic load, including a putative gamete-lethal mutation, triggering significant segregation distortion across 31.7% of the genome. We established that these distortion profiles are driven by the cumulative effects of multiple loci, with the magnitude of distortion depending on haplotype interactions. Collectively, our study quantifies the recombination landscape of apomixis and provides a framework for unmasking and mitigating genetic load in asexual crops.