Chemical composition of preen wax reflects major histocompatibility complex similarity in songbirds

Abstract

In jawed vertebrates, genes of the major histocompatibility complex (MHC) play a key role in immunity by encoding cell-surface proteins that recognize and bind non-self antigens. High variability at MHC suggests that these loci may also function in social signalling such as mate choice and kin recognition. This requires that MHC genotype covaries with some perceptible phenotypic trait. In mammals and fish, MHC is signalled chemically through volatile and non-volatile peptide odour cues, facilitating MHC-dependent mate choice and other behaviours. In birds, despite evidence for MHC-dependent mating, candidate mechanisms for MHC signalling remain largely unexplored. However, feather preen wax has recently been implicated as a potential source of odour cues. We examined whether the chemical composition of preen wax correlates with MHC class IIβ genotypes of wild song sparrows (Melospiza melodia). Pairwise chemical distance reflected amino acid distance at MHC for male-female dyads, although not for same-sex dyads. Chemical diversity did not reflect MHC diversity. We used gas chromatography-mass spectrometry (GC-MS) to characterize preen wax compounds, and identified four wax esters that best reflect MHC similarity. Provided songbirds can detect variation in preen wax composition, this cue may allow individuals to assess MHC compatibility of potential mates.

Plumage microbiota covaries with the major histocompatibility complex in blue petrels

“…Major histocompatibility complex genotype may indirectly influence feather microbiota via effects on the lipid composition of preen gland secretions (Leclaire, van Dongen, et al, ; Slade et al, ). These secretions, which birds regularly spread onto their plumage, have repeatedly been shown to limit the growth of some bacterial strains, while favouring others (Martin‐Platero et al, ; Shawkey, Pillai, & Hill, ; Verea, Vitelli–Flores, Isturiz, Rodríguez–Lemoine, & Bosque, ).…”

Extra‐pair mating in a passerine bird with highly duplicated major histocompatibility complex class II: Preference for the golden mean

“…The bluethroat has relatively few MHCI loci (i.e., four; O'Connor, Strandh, Hasselquist, Nilsson, & Westerdahl, 2016;Rekdal et al, 2018), which might be due to less exposure to intra-than extracellular pathogens (Minias et al, 2018) or some compensatory immunological mechanism (e.g., Gangoso et al, 2012;Star et al, 2011). Recent studies have identified a link between MHCII composition and individual odor in birds, possibly mediated through microbial communities and uropygial gland secretions (Leclaire et al, 2019(Leclaire et al, , 2014Leclaire, Strandh, Mardon, Westerdahl, & Bonadonna, 2017;Slade et al, 2016;Strandh et al, 2012). As there is growing evidence that birds are able to use olfaction in MHC-based mate choice, also in a selfreferencing manner (reviewed by Caro, Balthazart, & Bonadonna, 2015), MHCII is a prominent candidate for such a mate choice mechanism.…”

MHC‐mediated sexual selection on birdsong: Generic polymorphism, particular alleles and acoustic signals

“…In birds, despite a list of evidence for MHC‐dependent mating (e.g., Dunn et al., ; Griggio et al., ; von Schantz et al., ; Whittingham et al., ), candidate mechanisms for MHC signalling remain yet to be explored (Slade et al., , ). This strikingly contrasts with our knowledge in other vertebrate taxa.…”

“…Proximate mechanisms functioning in MHC‐mediated mate choice typically include odour signals in many animals, as MHC molecules can be bound to volatile chemicals that are excreted via the skin, urine or faeces thus can contribute to body odours (Carroll, Penn, & Potts, ; Milinski, Croy, Hummel, & Boehm, ; Milinski et al., ; Olsson et al., ; Penn, ). In birds, chemical signalling is still poorly recognized, but the secretion of the uropygial gland or feather microflora have recently been implicated as a potential source of scent cue for MHC signalling (Leclaire et al., ; Slade et al., ; Strandh et al., ), while olfactory perception has also been described at least in some species (Fracasso, Tuliozi, Hoi, & Griggio, ; Griggio, Fracasso, Mahr, & Hoi, ). In animals that only partially rely on olfactory cues, condition‐dependent visual or behavioural traits can signal genetic resistance, because only males with high immunocompetence (as determined by their MHC genotype) can bear the costs of elaborated sexual displays (Folstad & Karter, ; Hamilton & Zuk, ).…”