Spatio‐temporal variation in parasite communities maintains diversity at the major histocompatibility complex class IIβ in the endangered Rio Grande silvery minnow

Abstract

Climate change will strongly impact aquatic ecosystems particularly in arid and semi-arid regions. Fish-parasite interactions will also be affected by predicted altered flow and temperature regimes, and other environmental stressors. Hence, identifying environmental and genetic factors associated with maintaining diversity at immune genes is critical for understanding species' adaptive capacity. Here, we combine genetic (MHC class IIβ and microsatellites), parasitological and ecological data to explore the relationship between these factors in the remnant wild Rio Grande silvery minnow (Hybognathus amarus) population, an endangered species found in the southwestern United States. Infections with multiple parasites on the gills were observed and there was spatio-temporal variation in parasite communities and patterns of infection among individuals. Despite its highly endangered status and chronically low genetic effective size, Rio Grande silvery minnow had high allelic diversity at MHC class IIβ with more alleles recognized at the presumptive DAB1 locus compared to the DAB3 locus. We identified significant associations between specific parasites and MHC alleles against a backdrop of generalist parasite prevalence. We also found that individuals with higher individual neutral heterozygosity and higher amino acid divergence between MHC alleles had lower parasite abundance and diversity. Taken together, these results suggest a role for fluctuating selection imposed by spatio-temporal variation in pathogen communities and divergent allele advantage in maintenance of high MHC polymorphism. Understanding the complex interaction of habitat, pathogens and immunity in protected species will require integrated experimental, genetic and field studies.

The evolution of the major histocompatibility complex in upstream versus downstream river populations of the longnose dace

“…These nucleotide and amino acid sequences were verified as belonging to the MHC II β exon 2 DAB3 locus using BLAST searches. In searches optimized for highly similar sequences, our sequences aligned to the MHC II β exon 2 of blacknose dace ( Rhinichthys atratulus ) and longnose dace (Girard & Angers, ), and the DAB3 locus of the MHC II β exon 2 of a hybrid between two European cyprinids, Parachondrostoma toxostoma and Chondrostoma nasus (Pctn‐DAB3*40 allele; Šimková et al., ), indicating that the DAB3 locus was probably analyzed in a previous study on longnose dace MHC variation (Girard & Angers, ; as in Osborne, Pilger, Lusk, & Turner, ). Nearly all alleles were found in every river with the exception of allele 5, which was only found in the Milk River (Table ).…”

“…indicating that the DAB3 locus was probably analyzed in a previous study on longnose dace MHC variation (Girard & Angers, 2011;as in Osborne, Pilger, Lusk, & Turner, 2017). Nearly all alleles were found in every river with the exception of allele 5, which was only found in the Milk River (Table 2).…”

“…This result was obtained despite the fact that neutral diversity was comparable between the two studies, as above. From 542 individuals, only four MHC alleles and a total of 11 polymorphic sites were identified in that study; it was likely that only DAB3 was analyzed in that study (Girard & Angers, ; Osborne et al., ). BLAST searches revealed that no alleles were identical between our study and the Quebec longnose dace study, with alleles from our study differing from between one and five nucleotide substitutions from alleles from the Quebec study.…”

“…Other studies on cyprinids have shown strong positive selection on the second exon of the DAB3 locus (e.g., Collin, Burri, Comtesse, & Fumagalli, 2013;Ottová et al, 2005;Seifertová & Šimková, 2011), and whether DAB1 or DAB3 loci were more variable differed among species. In the North American Rio Grande silvery minnow (Hybognathus amarus), DAB1 had considerably more allelic diversity, with 55 alleles identified for DAB1 and only 13 alleles identified for DAB3 in a sample of 252 individuals (Osborne et al, 2017). Individuals each had ~1-2 alleles on average, with a maximum of four alleles in one individual (Osborne et al, 2017).…”

Specific MHC class I supertype associated with parasite infection and color morph in a wild lizard population

“…Evidence for parasite‐mediated selection acting on MHC genes via rare‐allele advantage (Borghans, Beltman, & De Boer, ; Schwensow et al., ), fluctuating selection (Jones, Cheviron, & Carling, ; Osborne, Pilger, Lusk, & Turner, ), heterozygote advantage (Doherty & Zinkernagel, ; Takahata & Nei, ), and optimal intermediate diversity advantage (Wegner, Kalbe, Kurtz, Reusch, & Milinski, ) has been uncovered across a range of taxa. However, most evidence points toward rare‐allele advantage and fluctuating selection as the dominant mechanisms by which pathogen‐mediated selection maintains MHC diversity, with little evidence that heterozygote advantage alone can account for the extreme diversity found at MHC loci (De Boer, Borghans, van Boven, Kesmir, & Weissing, ).…”