Self-referent MHC type matching in frog tadpoles

Abstract

Self/non-self recognition mechanisms underlie the development, immunology and social behaviour of virtually all living organisms, from bacteria to humans. Indeed, recognition processes lie at the core of how social cooperation evolved. Much evidence suggests that the major histocompatibility complex (MHC) both facilitates nepotistic interactions and promotes inbreeding avoidance. Social discrimination based on MHC differences has been demonstrated in many vertebrates but whether the labels used in discrimination are directly associated with the MHC, rather than with other genes with which it covaries, has remained problematic. Furthermore, effects of familiarity on natural preferences have not been controlled in most previous studies. Here we show that African clawed frog (Xenopus laevis) tadpoles discriminate among familiar full siblings based on MHC haplotype differences. Subjects (NZ261) from four parental crosses preferred siblings with which they shared MHC haplotypes to those with no MHC haplotypes in common. Using only full siblings in experimental tests, we controlled for genetic variation elsewhere in the genome that might influence schooling preferences. As test subjects were equally familiar with stimulus groups, we conclude that tadpole discrimination involves a self-referent genetic recognition mechanism whereby individuals compare their own MHC type with those of conspecifics.

Automated high-throughput measurement of body movements and cardiac activity of Xenopus tropicalis tadpoles

“…Importantly, we used these animals at pre-metamorphic stages with most of the organs and neuronal structures being developed and functional. These animals are capable of performing complex behavior trials and show learning abilities and social interactions [21,22,26,27,42,43]. Such features are mostly not established in embryos thus, favoring the tadpole model for experiments estimating effects on human health.…”

The hidden benefits of sex: Evidence for MHC‐associated mate choice in primate societies

“…If so, we need to understand how they discriminate kin. Recognition of familiar kin is typically credited to social learning, through stable bonds created during early development [37]. Identification of unfamiliar kin (such as paternal relatives when paternity uncertainty is high) may rely on alternative mechanisms, including self-referent phenotype matchingthe comparison between own and other's phenotype [38].…”

Social discrimination by quantitative assessment of immunogenetic similarity

“…We reared tadpoles with their siblings in groups of 200 within 40 l tanks for two to three weeks and fed them by maintaining a suspension of finely ground nettle. We determined the MHC haplotypes of all stimulus and subject tadpoles by the polymerase chain reaction (PCR) using sequence-specific primers [11] from tail tip tissue before behavioural tests. After taking tail clips, we isolated tadpoles in 1 l polypropylene cups for one to four weeks, during which time tadpoles' tails fully regenerated, and we then tested them.…”

“…Beyond that, inclusive fitness should be maximized by recognition of genetic similarity [2], possibly facilitated by special kin-recognition genes [3,4]. Some behaviours directly covary with genetic relatedness [5], and putative kin-recognition genes have been identified [6][7][8][9][10][11]. If such genes function to enable organisms to recognize kin, we expect to find that social behaviours, where discrimination is adaptive, vary in direct response to the signalling products of these genes [12].…”

“…However, frog tadpoles discriminate even among their siblings, specifically associating with others with which they share MHC haplotypes in preference to those that bear different haplotypes [11]. In Xenopus laevis, a model organism for studying vertebrate immunology [40], we tested whether social discrimination varies proportionally to quantifiable signal differences as determined by amino acid sequence similarity in the MHC -PBR.…”