Heterosis across environmental and genetic space

When genetically divergent lineages meet again in secondary contact, hybrids may suffer negative, fitness-reducing consequences, and benefit from positive genetic interactions that result in increased fitness. Empirical studies of heterosis, a phenomenon in which hybrids outperform their inbred progenitors, are of great interest in agriculture, but are less often performed in wild systems. In this study, we leverage Boechera retrofracta, a primarily self-fertilizing wildflower species, to explore how population divergence influences fitness effects upon secondary contact. We integrated genomic data and a large-scale fitness experiment to compare fitness and heterozygosity between outbred and inbred progeny of B. retrofracta. We show that interpopulation hybrids have increased overwintering survival compared to inbred individuals, indicative of heterosis. The magnitude of heterosis varied across genotypes and different environments, with overwintering survival increasing with genetic distance between parents. Sliding window analyses of genotyping by sequencing data show that heterozygosity varies across the genome of two species, B. retrofracta and the commonly co-occurring species Boechera stricta. We next compared these data with de novo F2s (intrapopulation, interpopulation, and interspecific crosses), as well as with wild-collected interpopulation cross B. retrofracta and interspecific B. stricta x B. retrofracta hybrids. Wild-collected interspecific hybrids appear to be F1s, while wild-collected intraspecific B. retrofracta are consistent with more complex crossing patterns. Because outcrossing is associated with a transition to asexuality in this group, this suggests different mechanisms underlie asexuality in hybrid and non-hybrid lineages. These findings underscore the potential differences in the role of heterosis between genetic groups at different stages of divergence and its relevance following hybridization in nature.