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Immune systems pose fascinating puzzles for evolutionary biologists. They feature some of the most polymorphic genes and reflect the strongest natural selection known. Evolution of immune systems plays a key role in host–parasite interactions, speciation, and eco-evolutionary dynamics that have community- and ecosystem-wide consequences. Conversely, evolutionary perspectives enrich our understanding of immunology, revealing macroevolutionary origins of key immune traits, their function in wild populations as opposed to sterile lab settings, and trade-offs that constrain immune adaptation. Here, we review key themes in the fast-growing interdisciplinary field of evolutionary immunology, focusing on multicellular animals. We describe macroevolution of immune functions, evidence of contemporary selection on immune genes, and the underlying theory seeking to explain this selection at multiple biological scales. We identify major open questions and opportunities in the field today. Foremost among these is the challenge of accurately and appropriately measuring relevant immune traits in wild and nonmodel organisms, which is necessary to understand their evolution in natural settings. A second challenge is to describe how diverse communities of symbionts impose selection on the highly multivariate and pleiotropic immune system. 

Studying the mechanisms underlying the genotype-phenotype association is crucial in genetics. Gene expression studies have deepened our understanding of the genotype  →  expression  →  phenotype mechanisms. However, traditional expression quantitative trait loci (eQTL) methods often overlook the critical role of gene co-expression networks in translating genotype into phenotype. This gap highlights the need for more powerful statistical methods to analyze genotype  →  network  →  phenotype mechanism. Here, we develop a network-based method, called spectral network quantitative trait loci analysis (snQTL), to map quantitative trait loci affecting gene co-expression networks. Our approach tests the association between genotypes and joint differential networks of gene co-expression via a tensor-based spectral statistics, thereby overcoming the ubiquitous multiple testing challenges in existing methods. We demonstrate the effectiveness of snQTL in the analysis of three-spined stickleback Gasterosteus aculeatus data. Compared to conventional methods, our method snQTL uncovers chromosomal regions affecting gene co-expression networks, including one strong candidate gene that would have been missed by traditional eQTL analyses. Our framework suggests the limitation of current approaches and offers a powerful network-based tool for functional loci discoveries. 

ABSTRACT Dispersal can affect individual‐level fitness and population‐level ecological and evolutionary processes. Factors that affect dispersal could therefore have important eco‐evolutionary implications. Here, we investigated the extent to which an inflammation and tissue repair response—peritoneal fibrosis—which is known to restrict movement, could influence dispersal by conducting a mark‐recapture experiment in a lake in Alaska with threespine stickleback (Gasterosteus aculatus). A subset of captured stickleback were injected with aluminium phosphate to experimentally induce fibrosis (‘treatment group’), and another subset were injected with saline or received no injection—both of which do not induce fibrosis (‘control group’). We released all fish at one introduction point and re‐sampled stickleback throughout the lake for 8 days. We recaptured 123 individuals (n = 47 fibrosis treatment;n = 76 control) and dissected them to determine fibrosis levels. Overall, fibrosis did not affect dispersal. Some compelling (but not statistically significant) trends suggest that early‐stage inflammation may affect dispersal, providing opportunities for future work. By showing that effects on dispersal are not important side effects of fibrosis, these findings improve our understanding of the ecological implications of immune responses. 

ABSTRACT Commensal microbial communities have immense effects on their vertebrate hosts, contributing to a number of physiological functions, as well as host fitness. In particular, host immunity is strongly linked to microbiota composition through poorly understood bi-directional links. Gene expression may be a potential mediator of these links between microbial communities and host function. However, few studies have investigated connections between microbiota composition and expression of host immune genes in complex systems. Here, we leverage a large study of laboratory-raised fish from the species Gasterosteus aculeatus (three-spined stickleback) to document correlations between gene expression and microbiome composition. First, we examined correlations between microbiome alpha diversity and gene expression. Our results demonstrate robust positive associations between microbial alpha diversity and expression of host immune genes. Next, we examined correlations between host gene expression and abundance of microbial taxa. We identified 15 microbial families that were highly correlated with host gene expression. These families were all tightly correlated with host expression of immune genes and processes, falling into one of three categories—those positively correlated, negatively correlated, and neutrally related to immune processes. Furthermore, we highlight several important immune processes that are commonly associated with the abundance of these taxa, including both macrophage and B cell functions. Further functional characterization of microbial taxa will help disentangle the mechanisms of the correlations described here. In sum, our study supports prevailing hypotheses of intimate links between host immunity and gut microbiome composition. IMPORTANCE Here, we document associations between host gene expression and gut microbiome composition in a nonmammalian vertebrate species. We highlight associations between expression of immune genes and both microbiome diversity and abundance of specific microbial taxa. These findings support other findings from model systems which have suggested that gut microbiome composition and host immunity are intimately linked. Furthermore, we demonstrate that these correlations are truly systemic; the gene expression detailed here was collected from an important fish immune organ (the head kidney) that is anatomically distant from the gut. This emphasizes the systemic impact of connections between gut microbiota and host immune function. Our work is a significant advancement in the understanding of immune-microbiome links in nonmodel, natural systems.