HighMHCdiversity confers no advantage for phenotypic quality and reproductive performance in a wild bird

Abstract

Genes of the major histocompatibility complex (MHC) encode antigen‐binding molecules and are an integral part of the acquired immune response of vertebrates. In general, high individual MHC diversity is expected to increase fitness by broadening the spectrum of pathogens recognized by the immune system, in accordance with the heterozygote advantage mechanism. On the other hand, the optimality hypothesis assumes that individuals with optimal (intermediate), rather than maximum, diversity of the MHC will achieve the highest fitness because of inherent costs associated with expressing diverse MHC alleles. Here, we tested for associations between individual diversity of the MHC class I and class II genes (binding antigens of intra‐ and extracellular pathogens respectively) and a range of fitness‐related traits (condition, ornament expression and reproduction) in an urban population of the Eurasian coot Fulica atra. Contrary to our expectation, we found that high within‐individual allelic diversity of MHC genes (both class I and II) was associated with poorer condition (lower blood haemoglobin concentrations), weaker expression of the putative ornament (smaller frontal shield), later onset of breeding and smaller clutches. An analysis of functional MHC allele clusters (supertypes) provided further support for negative associations of MHC diversity with phenotypic quality and reproductive performance, but most of these relationships could not be explained by the presence of specific maladaptive supertypes. Finally, we found little empirical support for the optimality hypothesis in the Eurasian coot. Our results suggest that the costs of high MHC diversity outweighed any benefits associated with broad MHC repertoire, which could be driven by depauperate pathogen diversity in an urban landscape. To the best of our knowledge, this is one of the first studies providing consistent evidence for negative associations of MHC diversity with a range of fitness‐related traits in a natural avian population.

MHC diversity associates with reproductive success in a bird species with biparental care

“…Theoretical models of pathogen-mediated selection and most of the empirical evidence support that higher MHC diversity induce higher individual performance. However, our findings are in line with the growing evidence supporting also for a negative association between MHC divergence and fitness-related traits (e.g., Acevedo-Whitehouse et al, 2018;Gagnon et al, 2020;Ilmonen et al, 2007;Lukasch et al, 2017;Pikus et al, 2022). Three alternative hypotheses could explain why lower MHC divergence can result in higher fledging success.…”

“…Overall, these findings are in line with previous studies in birds reporting no evidence for an association of MHC and clutch size (Sawada et al, 2020;Sepil et al, 2013a;Sun et al, 2019). As an exception, it was observed in Eurasian coot (Fulica atra) that individuals with low and intermediate levels of MHC-I and MHC-II diversity, respectively, laid larger clutches (Pikus et al, 2022). However, whether these effects are only additive at the couple level remain to be addressed.…”

“…Third, selective pressures imposed by various pathogens can be limited in this barn owl population. Due to the energetic costs of mounting immune responses, it is possible that carrying less divergent alleles is already the optimal level of divergence given lower pressure imposed by a less diverse community of parasites (Goüy De Bellocq et al, 2008;Pikus et al, 2022;Radwan et al, 2014). Considering our results, we speculate that selection is acting against individuals with higher level of functional divergence at MHC-Iα loci through a decrease in reproductive fitness potentially reflecting a trade-off between current reproductive effort and self-maintenance (Bonneaud et al, 2004;Roved et al, 2018).…”

“…Several studies have shown an association between MHC variation and reproductive success (e.g., Hoover et al, 2018;Huang et al, 2022;Kalbe et al, 2009;Lenz et al, 2013;Pikus et al, 2022;Roved et al, 2018;Sepil et al, 2013a). For instance, specific MHC-I supertypes explained higher reproductive success in great tits, Parus major ( Sepil et al, 2013a), whereas in the Galápagos sea lions, Zalophus wollebaeki, MHC-II divergence was involved instead (Lenz et al, 2013).…”

“…For instance, specific MHC-I supertypes explained higher reproductive success in great tits, Parus major ( Sepil et al, 2013a), whereas in the Galápagos sea lions, Zalophus wollebaeki, MHC-II divergence was involved instead (Lenz et al, 2013). However, these studies usually targeted only one component of the MHC adaptive immunity, either MHC-I or MHC-II (but see Pikus et al, 2022). Given that genes of different MHC classes are responsible for the detection of pathogens of different nature and thus, under different selective pressures (Minias et al, 2018), a multi-locus approach is needed to better understand the extent of MHC-fitness associations (A Gaigher et al, 2019;Kamiya et al, 2014).…”