Abstract

All organisms encounter pathogens, and birds are especially susceptible to infection by malaria parasites and other haemosporidians. It is important to understand how immune genes, primarily innate immune genes which are the first line of host defense, have evolved across birds, a highly diverse group of tetrapods. Here, we find that innate immune genes are highly conserved across the avian tree of life and that although most show evidence of positive or diversifying selection within specific lineages or clades, the number of sites is often proportionally low in this broader context of putative constraint. Rather, the evidence shows a much higher level of negative or purifying selection in these innate immune genes - rather than adaptive immune genes - which is consistent with birds' long coevolutionary history with pathogens and the need to maintain a rapid response to infection. We further explored avian responses to haemosporidians by comparing differential gene expression in wild birds (1) uninfected with haemosporidians, (2) infected with Plasmodium, and (3) infected with Haemoproteus (Parahaemoproteus). We found patterns of significant differential expression with some genes unique to infection with each genus and a few shared between "treatment" groups, but none that overlapped with the genes included in the phylogenetic study.

Highlights

  • Our understanding of the evolution of the avian genome has recently been updated by the landmark avian phylogenomic paper by Jarvis et al (2014)

  • Birds as a whole appear to have evolved at a conservative molecular evolutionary rate when contrasted with other large groups of organisms, passeriform songbirds have an average mutation rate that is close to twice that of other avian species (Jarvis et al, 2014; Zhang et al, 2014)

  • We included most pattern-recognition receptors (PRRs) that we could align with at least 250 base pairs, some non-PRR genes and some from the adaptive immune system with at least 250 bp; we did not include all the Toll-like receptors (TLR) because they had been analysed in another study (Grueber et al, 2014)

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Summary

Introduction

Our understanding of the evolution of the avian genome has recently been updated by the landmark avian phylogenomic paper by Jarvis et al (2014) This phylogeny includes all extant orders from Neoaves (e.g. songbirds, parrots, pigeons) and species from several clades in the more basal orders including Anseriformes (waterfowl), Galliformes (landfowl), Tinamiformes (tinamous) and Struthioniformes (ostrich). The phylogeny supports the rapid radiation of the most derived order Passeriformes (i.e. perching birds) and their sister taxon, the parrots (Psittaciformes). This diversification occurred around 60–55 million years ago during the Late Paleocene in Gondwana (Gill, 1995; Jarvis et al, 2014). Birds as a whole appear to have evolved at a conservative molecular evolutionary rate when contrasted with other large groups of organisms (notably mammals), passeriform songbirds have an average mutation rate that is close to twice that of other avian species (Jarvis et al, 2014; Zhang et al, 2014)

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