Combining molecular evolution and environmental genomics to unravel adaptive processes of MHC class IIB diversity in European minnows (Phoxinus phoxinus)

Helene Collin,Fabien Comtesse,Reto Burri,Luca Fumagalli

doi:10.1002/ece3.650

Abstract

Host–pathogen interactions are a major evolutionary force promoting local adaptation. Genes of the major histocompatibility complex (MHC) represent unique candidates to investigate evolutionary processes driving local adaptation to parasite communities. The present study aimed at identifying the relative roles of neutral and adaptive processes driving the evolution of MHC class IIB (MHCIIB) genes in natural populations of European minnows (Phoxinus phoxinus). To this end, we isolated and genotyped exon 2 of two MHCIIB gene duplicates (DAB1 and DAB3) and 1′665 amplified fragment length polymorphism (AFLP) markers in nine populations, and characterized local bacterial communities by 16S rDNA barcoding using 454 amplicon sequencing. Both MHCIIB loci exhibited signs of historical balancing selection. Whereas genetic differentiation exceeded that of neutral markers at both loci, the populations' genetic diversities were positively correlated with local pathogen diversities only at DAB3. Overall, our results suggest pathogen-mediated local adaptation in European minnows at both MHCIIB loci. While at DAB1 selection appears to favor different alleles among populations, this is only partially the case in DAB3, which appears to be locally adapted to pathogen communities in terms of genetic diversity. These results provide new insights into the importance of host–pathogen interactions in driving local adaptation in the European minnow, and highlight that the importance of adaptive processes driving MHCIIB gene evolution may differ among duplicates within species, presumably as a consequence of alternative selective regimes or different genomic context.Using next-generation sequencing, the present manuscript identifies the relative roles of neutral and adaptive processes driving the evolution of MHC class IIB (MHCIIB) genes in natural populations of a cyprinid fish: the European minnow (Phoxinus phoxinus). We highlight that the relative importance of neutral versus adaptive processes in shaping immune competence may differ between duplicates as a consequence of alternative selective regimes or different genomic contexts.

Highlights

In natural environments, heterogeneity in selection due to habitat fragmentation, climate fluctuations, and pathogen regime variation play a major role in shaping populations’ genetic diversity, and eventually can lead to local adaptation (Kawecki and Ebert 2004; Sommer 2005; Barrett et al 2008; Gandon and Nuismer 2009; Spurgin and Richardson 2010)
All MHC class IIB (MHCIIB) sequences obtained by cloning four individuals of six P. phoxinus populations blasted against previously published MHCIIB sequences of other cyprinids and salmonids (S. salar), with sequence similarities ranging from 79% to 92%
Functionality of the genes was supported by successful cDNA amplification (Text S1), and orthology with DAB1 and DAB3 of other cyprinids was confirmed by two well-separated paralog sequence clusters in a phylogenetic analysis (Appendix 1), with alleles from different species found in each duplicate cluster

Summary

Introduction

Heterogeneity in selection due to habitat fragmentation, climate fluctuations, and pathogen regime variation play a major role in shaping populations’ genetic diversity, and eventually can lead to local adaptation (Kawecki and Ebert 2004; Sommer 2005; Barrett et al 2008; Gandon and Nuismer 2009; Spurgin and Richardson 2010). Pathogen communities can affect various fitness traits linked to immune resistance in hosts (Summers et al 2003; Simkova et al 2006; Evans and Neff 2009). Hosts develop a wide range of immune responses to overcome pathogen infections (Acevedo-Whitehouse and Cunningham 2006). Host– pathogen interactions are ideal to study local adaptation, as both host and pathogen are subjected to varying selection in time and space, modifying their reciprocal fitness. Genes of the major histocompatibility complex (MHC) are among the best candidates to study the genetics of the adaptive immune response (e.g., Klein 1987; Kalz and Shykoff 1998; Piertney and Oliver 2006). MHC genes are the most polymorphic genes in vertebrates, and participate in the activation of the adaptive immune response (Klein 1986).

Methods

Results

Discussion

Conclusion