Spatial and temporal variation at major histocompatibility complex class IIB genes in the endangered Blakiston’s fish owl

Abstract

IntroductionQuantifying intraspecific genetic variation in functionally important genes, such as those of the major histocompatibility complex (MHC), is important in the establishment of conservation plans for endangered species. The MHC genes play a crucial role in the vertebrate immune system and generally show high levels of diversity, which is likely due to pathogen-driven balancing selection. The endangered Blakiston’s fish owl (Bubo blakistoni) has suffered marked population declines on Hokkaido Island, Japan, during the past several decades due to human-induced habitat loss and fragmentation. We investigated the spatial and temporal patterns of genetic diversity in MHC class IIβ genes in Blakiston’s fish owl, using massively parallel pyrosequencing.ResultsWe found that the Blakiston’s fish owl genome contains at least eight MHC class IIβ loci, indicating recent gene duplications. An analysis of sequence polymorphism provided evidence that balancing selection acted in the past. The level of MHC variation, however, was low in the current fish owl populations in Hokkaido: only 19 alleles were identified from 174 individuals. We detected considerable spatial differences in MHC diversity among the geographically isolated populations. We also detected a decline of MHC diversity in some local populations during the past decades.ConclusionsOur study demonstrated that the current spatial patterns of MHC variation in Blakiston’s fish owl populations have been shaped by loss of variation due to the decline and fragmentation of populations, and that the short-term effects of genetic drift have counteracted the long-term effects of balancing selection.Electronic supplementary materialThe online version of this article (doi:10.1186/s40851-015-0013-4) contains supplementary material, which is available to authorized users.

Duplication and Variation in the Major Histocompatibility Complex Genes in Blakiston's Fish Owl, Bubo blakistoni

“…The B. blakistoni populations could have experienced severe bottlenecks during glacial periods, which could have reduced genetic variation. In addition, recent population fragmentation and decline owing to human activities has resulted in decreased genetic variation , and the level of MHCIIβ variation has decreased in the B. blakistoni population on Hokkaido Island during the past decades (Kohyama et al, 2015). However, the number of MHCIIβ alleles per individual remains large among owl species (Table 1), probably because of multiple loci.…”

“…We utilized sequence data from Kohyama et al (2015), who obtained partial sequences (203 bp) of MHCIIβ exon 2 from 174 B. blakistoni individuals sampled on Hokkaido Island, by massively parallel pyrosequencing. In addition, sequences were obtained from one individual of B. flavipes, and two individuals each of B. bubo, B. virginianus, and B. scandiacus, by the same method as in Kohyama et al (2015). Briefly, pyrosequencing was performed on PCR products obtained from genomic DNA by using the primer set BublIIb2F (5′-GAG TGT CAG YAC CTY RAY RG-3′) and BublIIb2R (5′-CTT TCY TCT SCS TGA YGW AGG-3′).…”

“…The population of B. blakistoni on Hokkaido Island, Japan, decreased in the 20th century, resulting in low genetic diversity at present . Recently, Kohyama et al (2015) reported up to 16 different MHCIIβ alleles per individual in B. blakistoni based on the next-generation sequencing approach. This indicates that the B. blakistoni genome contains at least eight copies of MHCIIβ genes, the highest number of gene copies reported in a non-passerine bird.…”

“…Sample sizes, chromosome number(Rebholz et al, 1993) and numbers of MHC class IIβ alleles per individual detected by massively parallel pyrosequencing. The pyrosequencing data for B. blakistoni are fromKohyama et al (2015). TIK conducted massively parallel pyrosequencing.…”

Effects of parasite and historic driven selection on the diversity and structure of a MHC-II gene in a small mammal species (Peromyscus leucopus) undergoing range expansion

“…Genetic diversity across populations of a species is generally not homogeneously distributed throughout the species range, and distinct processes drive such heterogeneity (Johansson et al 2006;Eckert et al 2008;Excoffier et al 2009;Adams and Hadly 2012;Lau et al 2014;Chen et al 2015;Kohyama et al 2015). The central marginal hypothesis (Prakash et al 1969;Brussard 1984) states that genetic diversity decreases from the core to the margin of a species distribution range, with effective population size and gene flow decreasing in populations towards the range margin.…”