The evolution of immunity in relation to colonization and migration

Abstract

Colonization and migration have a crucial effect on patterns of biodiversity, with disease predicted to play an important role in these processes. However, evidence of the effect of pathogens on broad patterns of colonization and migration is limited. Here, using phylogenetic analyses of 1,311 species of Afro-Palaearctic songbirds, we show that colonization events from regions of high (sub-Saharan Africa) to low (the Palaearctic) pathogen diversity were up to 20 times more frequent than the reverse, and that migration has evolved 3 times more frequently from African- as opposed to Palaearctic-resident species. We also found that resident species that colonized the Palaearctic from Africa, as well as African species that evolved long-distance migration to breed in the Palaearctic, have reduced diversity of key immune genes associated with pathogen recognition (major histocompatibility complex class I). These results suggest that changes in the pathogen community that occur during colonization and migration shape the evolution of the immune system, potentially by adjusting the trade-off between the benefits of extensive pathogen recognition and the costs of immunopathology that result from high major histocompatibility complex class I diversity.

Reconstructing the geographic and climatic origins of long‐distance bird migrations

“…These results support the idea that strong climatic seasonality has been an important factor in the evolution of long-distance bird migration (see Winger et al, 2019;Zink & Gardner, 2017). However, more in-depth studies are needed to confirm and understand the effect of different drivers on the evolution of long-distance migration, ideally by considering several environmental factors (see O'Connor et al, 2018;Somveille, Manica, et al, 2018) and by using clades with well-resolved phylogenies.…”

“…For instance, the migration distances of species breeding in very seasonal local environments within temperate latitudes (between latitudes 50° and 30° and −30° and −50°) are as long as, and sometimes longer tFFhan, the migration distances of some species breeding in Arctic latitudes (results not shown). However, more in-depth studies are needed to confirm and understand the effect of different drivers on the evolution of long-distance migration, ideally by considering several environmental factors (see O'Connor et al, 2018;Somveille, Manica, et al, 2018) and by using clades with well-resolved phylogenies. These results support the idea that strong climatic seasonality has been an important factor in the evolution of long-distance bird migration (see Winger et al, 2019;Zink & Gardner, 2017).…”

“…This phenomenon of geographic disjunction between the breeding and wintering ranges of certain species has long invited investigations regarding the physiology, behaviour and navigation of migratory birds (see Alerstam, Hedenström, & Åkesson, 2003;Gwinner & Helm, 2003;Newton, 2008;Pulido, 2007). Yet, the conditions that triggered the evolution of seasonal migration behaviour remain poorly understood, and seem to include both abiotic and biotic drivers, such as seasonal habitat quality and trophic resources, escape from predators, pathogens or competitor avoidance (Alerstam et al, 2003;O'Connor, Cornwallis, Hasselquist, Nilsson, & Westerdahl, 2018;Somveille, Rodrigues, & Manica, 2018).…”

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

“…This is in line with the theoretical framework of a trade‐off between recognizing a broad array of pathogens, and increased depletion of circulating T‐cells following negative selection in the thymus and risk of autoimmune diseases with increased number of MHC alleles (e.g., Gough & Simmonds, ; Nowak et al, ; Woelfing et al, ). What level of intraindividual MHC diversity that constitutes the optimum might vary among species due to ecological differences, e.g., according to the pathogen load experienced (Minias et al, ; O'Connor, Cornwallis, Hasselquist, Nilsson, & Westerdahl, ; Westerdahl et al, ). This implies that the more pathogens a species is exposed to, the stronger the selective force for increased diversity will be, driving the optimum towards a higher diversity.…”

Infection risk and extensive parental care govern the molecular evolution of Toll-like receptors in birds

“…Despite recent advances (Minias, et al 2017;O'Connor, et al 2018), it remains generally 72 unknown how pathogen-mediated selection affects immune gene evolution across species. Do signatures of positive selection mostly evolve convergent, or do they evolve divergent 74 depending on pathogen exposure and life-history trade-offs?…”