Social discrimination by quantitative assessment of immunogenetic similarity

Abstract

Genes of the major histocompatibility complex (MHC) that underlie the adaptive immune system may allow vertebrates to recognize their kin. True kin-recognition genes should produce signalling products to which organisms can respond. Allelic variation in the peptide-binding region (PBR) of MHC molecules determines the pool of peptides that can be presented to trigger an immune response. To examine whether these MHC peptides also might underlie assessments of genetic similarity, we tested whether Xenopus laevis tadpoles socially discriminate between pairs of siblings with which they differed in PBR amino acid sequences. We found that tadpoles (four sibships, n = 854) associated preferentially with siblings with which they were more similar in PBR amino acid sequence. Moreover, the strength of their preference for a conspecific was directly proportional to the sequence similarity between them. Discrimination was graded, and correlated more closely with functional sequence differences encoded by MHC class I and class II alleles than with numbers of shared haplotypes. Our results thus suggest that haplotype analyses may fail to reveal fine-scale behavioural responses to divergence in functionally expressed sequences. We conclude that MHC-PBR gene products mediate quantitative social assessment of immunogenetic similarity that may facilitate kin recognition in vertebrates.

Figure 1.

Association preference of subjects for the more immunogenetically similar stimulus group as a function of the MHC ‘stimulus differential’ between the two stimulus groups based on MHC class I (circles) and MHC class II PBR (squares) amino acid sequence similarity. The stimulus differential between each subject and the two stimulus groups was determined by subtracting the per cent amino acid similarity of the less MHC-similar stimulus group from that of the more MHC-similar stimulus group. Means ± s.e.m. are shown.

Figure 2.

Mean MHC-similarity preferences of MHC-homozygous subjects (four genotypes: ff, gg, jj and rr) among stimulus groups with different numbers of shared MHC haplotypes (2 versus 0 shared haplotypes; 2 versus 1 shared haplotypes; 1 versus 0 shared haplotypes). (a) Subjects spent more time associating with siblings sharing both MHC haplotypes than with siblings sharing no MHC haplotypes (2 versus 0). (b) Subjects spent more time associating with siblings sharing both MHC haplotypes than with siblings sharing only one MHC haplotype (2 versus 1). (c) Subjects did not differ in time associating with siblings sharing one or no MHC haplotypes (1 versus 0). Means ± s.e.m. are shown. *p < 0.05, **p < 0.001 (two-tailed).