Abstract
Understanding how wild immune variation covaries with other traits can reveal how costs and trade‐offs shape immune evolution in the wild. Divergent life history strategies may increase or alleviate immune costs, helping shape immune variation in a consistent, testable way. Contrasting hypotheses suggest that shorter life histories may alleviate costs by offsetting them against increased mortality, or increase the effect of costs if immune responses are traded off against development or reproduction. We investigated the evolutionary relationship between life history and immune responses within an island radiation of three‐spined stickleback, with discrete populations of varying life histories and parasitism. We sampled two short‐lived, two long‐lived and an anadromous population using qPCR to quantify current immune profile and RAD‐seq data to study the distribution of immune variants within our assay genes and across the genome. Short‐lived populations exhibited significantly increased expression of all assay genes, which was accompanied by a strong association with population‐level variation in local alleles and divergence in a gene that may be involved in complement pathways. In addition, divergence around the eda gene in anadromous fish is likely associated with increased inflammation. A wider analysis of 15 populations across the island revealed that immune genes across the genome show evidence of having diverged alongside life history strategies. Parasitism and reproductive investment were also important sources of variation for expression, highlighting the caution required when assaying immune responses in the wild. These results provide strong, gene‐based support for current hypotheses linking life history and immune variation across multiple populations of a vertebrate model.
Highlights
Parasitism is ubiquitous in nature (Poulin & Morand, 2000; Windsor, 1998), and variation in immune responses amongst wild populations is extensive at the phenotypic and genotypic level (Martin, Hawley, & Ardia, 2011; Pedersen & Babayan, 2011)
We have documented consistent population‐level variation in immune gene expression associated with life history strategies
There exists a relationship across the North Uist radiation between genetic variation around a large number of immune genes and evolved life history strategies
Summary
Parasitism is ubiquitous in nature (Poulin & Morand, 2000; Windsor, 1998), and variation in immune responses amongst wild populations is extensive at the phenotypic and genotypic level (Martin, Hawley, & Ardia, 2011; Pedersen & Babayan, 2011). We expand the analysis to a larger group of populations and assess the comparative relationship between life history strategy and genetic variation around a large number of immune genes across the genome Such an approach introduces a novel level of genetic accountability for immune covariance with life history that will help reveal the potential for evolutionary constraints or associations to occur. Stickleback are hosts to a plethora of parasites (De Roij & MacColl, 2012; MacColl, 2009; Poulin, Blanar, Thieltges, & Marcogliese, 2011; Young & MacColl, 2017), which have helped drive immune variation between wild freshwater populations (De Roij, Harris, & MacColl, 2011; Robertson, Bradley, & MacColl, 2016a,b; Scharsack, Kalbe, Harrod, & Rauch, 2007) This system allows us to ask questions about covariation between life history and immune phenotypes across multiple populations within a single radiation, promoting our understanding of how life history and immune responses diverge alongside one another. This may suggest that the anadromous population has the “longest” life history; such an interpretation is potentially confounded by the addition of migration between marine and saltwater inland lochs
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