Wetter climates select for higher immune gene diversity in resident, but not migratory, songbirds

Abstract

Pathogen communities can vary substantially between geographical regions due to different environmental conditions. However, little is known about how host immune systems respond to environmental variation across macro-ecological and evolutionary scales. Here, we select 37 species of songbird that inhabit diverse environments, including African and Palaearctic residents and Afro-Palaearctic migrants, to address how climate and habitat have influenced the evolution of key immune genes, the major histocompatibility complex class I (MHC-I). Resident species living in wetter regions, especially in Africa, had higher MHC-I diversity than species living in drier regions, irrespective of the habitats they occupy. By contrast, no relationship was found between MHC-I diversity and precipitation in migrants. Our results suggest that the immune system of birds has evolved greater pathogen recognition in wetter tropical regions. Furthermore, evolving transcontinental migration appears to have enabled species to escape wet, pathogen-rich areas at key periods of the year, relaxing selection for diversity in immune genes and potentially reducing immune system costs.

Keywords: birds; climate; immune genes; major histocompatibility complex; pathogens.

Figure 1.

Heatmaps of the distribution ranges of the Palaearctic and African resident species in the study (a) and the breeding and wintering ranges of the migratory species (b). Colours indicate the number of overlapping species. Each point represents a single species. Distribution maps provided by BirdLife international and Handbook of the Birds of the World (2017). Median monthly precipitation (c, mm) and temperature (d, °C) across the Palaearctic and Africa. The intensity of colour is proportional to the levels of precipitation and temperature. Climate data from monthly weather records (1901–2017) collated by the CRU at the University of East Anglia. (Online version in colour.)

Figure 2.

Relationship between the median monthly precipitation and the mean number of MHC-I alleles per individual in African residents (a) and Palaearctic residents (b). Relationship between median monthly temperature and the mean number of MHC-I alleles per individual in African residents (c) and Palaearctic residents (d). Each point represents a single species. Dashed lines and shaded areas show linear regressions with 95% confidence intervals. (Online version in colour.)

Figure 3.

Relationship between median monthly precipitation and the number of MHC-I alleles in Palaearctic residents and migrants in their Palaearctic breeding grounds (a). Relationship between median monthly precipitation and the number of MHC-I alleles in African residents and migrants in their African wintering grounds (b). Each point represents a single species. Dashed lines and shaded areas show linear regressions with 95% confidence intervals. (Online version in colour.)

Figure 4.

Relationship in the African residents between the number of MHC-I alleles and precipitation during the period when the migrants are also present in Africa (November–January). The dashed line and shaded area shows linear regressions with 95% confidence intervals. Each point represents a single species. (Online version in colour.)