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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 Recombination is central to genetics and to evolution of sexually reproducing organisms. However, obtaining accurate estimates of recombination rates, and of how they vary along chromosomes, continues to be challenging. To advance our ability to estimate recombination rates, we present Hi-reComb, a new method and software for estimation of recombination maps from bulk gamete chromosome conformation capture sequencing (Hi-C). Simulations show that Hi-reComb produces robust, accurate recombination landscapes. With empirical data from sperm of five fish species we show the advantages of this approach, including joint assessment of recombination maps and large structural variants, map comparisons using bootstrap, and workflows with trio phasing vs. Hi-C phasing. With off-the-shelf library construction and a straightforward rapid workflow, our approach will facilitate routine recombination landscape estimation for a broad range of studies and model organisms in genetics and evolutionary biology. Hi-reComb is open-source and freely available at https://github.com/millanek/Hi-reComb. 

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 Many terrestrial ectotherms have gone to great evolutionary lengths to adapt to long cold winters; some have even evolved the ability to tolerate the freezing of most of the extracellular fluid in the body. Now, however, high‐elevation and high‐latitude winters are experiencing an accelerated period of warming. Specialised winter adaptations that promoted fitness in a seasonally frozen environment may soon be superfluous or even maladaptive. We ask whether winter adaptations include changes in immune functions, and whether changing winter conditions could exert disparate effects on populations of a wide‐ranging terrestrial ectotherm, the wood frog (Lithobates sylvaticus). By rearing wood frogs from ancestral winter environments that vary in length and temperature in a common garden, and reciprocally exposing post‐metamorphic frogs to unfrozen and frozen artificial winter conditions in the lab, we were able to decompose transcriptomic differences in ventral skin gene expression into those that were environmentally induced (responsive to temperature) and genetically determined and those that varied as an interaction between the genotype and environment. We found that frogs from harsh ancestral winter environments constitutively upregulated immune processes, including cellular immunity, inflammatory processes and adaptive immune processes, as compared to frogs from mild ancestral winter environments. Further, we saw that the expression of several genes varied in an interaction between the genotype and artificial winter. We suggest that just as winter climates likely served as the selective force resulting in remarkable winter adaptations such as freeze tolerance, they may have also induced constitutive changes in immune gene expression. 

Abstract Most studies assessing rates of phenotypic change focus on population mean trait values, whereas a largely overlooked additional component is changes in population trait variation. Theoretically, eco‐evolutionary dynamics mediated by such changes in trait variation could be as important as those mediated by changes in trait means. To date, however, no study has comprehensively summarised how phenotypic variation is changing in contemporary populations. Here, we explore four questions using a large database: How do changes in trait variances compare to changes in trait means? Do different human disturbances have different effects on trait variance? Do different trait types have different effects on changes in trait variance? Do studies that established a genetic basis for trait change show different patterns from those that did not? We find that changes in variation are typically small; yet we also see some very large changes associated with particular disturbances or trait types. We close by interpreting and discussing the implications of our findings in the context of eco‐evolutionary studies.