Long-term balancing selection for pathogen resistance maintains trans-species polymorphisms in a planktonic crustacean
Balancing selection is an evolutionary process that maintains genetic polymorphisms at selected loci and strongly reduces the likelihood of allele fixation. When allelic polymorphisms predate speciation events and these polymorphisms are maintained independently in the resulting lineages, a pattern of trans-species polymorphisms (TSPs) may occur. TSPs have been identified mainly for loci related to mating systems and infectious diseases (e.g. MHC), but they are generally rare. TSP in disease loci are believed to be a consequence of long-term host–parasite coevolution by balancing selection, the so-called Red Queen dynamics. Here we scanned the genomes of three crustacean species with a divergence of over 15-million-years and identified 11 genes containing identical-by-descent SNPs with the same polymorphisms in all three species. Four of these genes display exceptional variability and molecular footprints of balancing selection. Among these gene candidates, which include genes related to immunity function, three were located in or in close proximity to loci involved in resistance to a virulent bacterial pathogen, Pasteuria, with which the Daphnia host is known to coevolve. This provides rare evidence of TSPs for loci known to be functionally relevant in interactions with a widespread and highly specific parasite. These findings support the theory that specific antagonistic coevolution is able to maintain genetic diversity over millions of years.