Effective Purging and Conservation of Heterozygous Regions During Independent Evolution to High‐Level Inbreeding in Wild Paradise Fishes

ABSTRACT Inbreeding may initially lower population fitness by converting masked genetic load into realised load. As deleterious variants become increasingly homozygous, purifying selection acts more effectively to purge load. Nevertheless, not all populations can survive the initial fitness decline, and it would be interesting to examine scenarios that facilitate their survival. Herein, we assembled chromosome‐level reference genomes of two paradise fishes, Macropodus hongkongensis and M. opercularis , and resequenced 109 wild individuals of 15 populations to infer the history of runs of homozygosity (ROH) formation, effectiveness of purging in ROH, and the role of balancing selection in maintaining lingering polymorphisms in independently evolved small populations. While the two species diverged in genes potentially adaptive to their local niches, there were large variations in inbreeding coefficients and the amount of genetic load within species. Three populations became highly inbred ( F ROH  > 0.50) from independent origins. Simulations showed that the ROH segment size distribution can be best explained by living in a small population for hundreds, if not thousands, of generations. The genetic load negatively correlated with summed ROH length. This was driven by more effective purging in ROH. The non‐ROH regions between individuals from different high‐ F ROH populations were repeatable, with nearby signals of balancing selection persisting in the polymorphic genomic regions through species divergence.