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The Major Histocompatibility Complex (MHC) genes encode proteins that initiate the adaptive immune response by presenting pathogen‐derived antigenic peptides to T lymphocytes. Host–pathogen coevolution drives MHC polymorphism, introducing intraspecific variation in host life expectancy. This variation interacts with optimal growth strategy, as growth increases reproductive potential. While mortality rate and body size‐dependent fecundity are major factors shaping life histories, the effect of intraspecific variation in MHC‐based immunity on the evolution of growth strategies and host body size remains unknown.Here, we model how host MHC–pathogen coevolution—and its concomitant impact on host mortality—can affect the evolution of host life histories, as represented by age at maturation and body size. Life histories were compared in scenarios with and without adaptive immune response under equal population‐level mortality rates.We show that host–pathogen coevolutionary dynamics selects for postponed maturation and increased body size. Although MHC genes and genes that determine body size were physically unlinked, selection imposed by the Red Queen process generated linkage disequilibrium between immunocompetent MHC alleles and the maturation‐postponing alleles that prolong growth phase and increase body size. Particularly large body size was attained when pathogens mutated slowly, thus allowing the advantage of resistant MHC alleles to persist over multiple generations.The emergence of adaptive immunity, which is pathogen‐specific and enables immunological memory, is considered a major evolutionary innovation of vertebrates. Our work suggests that the adaptive immune response, mediated by polymorphic MHC genes, may drive the evolution of host body size. This form of adaptive immunity may have thus predisposed vertebrates to evolve large body size and exhibit the macroevolutionary patterns of increasing body size over time that have been detected in comparative studies. Read the free Plain Language Summary for this article on the Journal blog. [ABSTRACT FROM AUTHOR]

In many annual plants, mollusks, crustaceans and ectothermic vertebrates, growth accompanies reproduction. The growth curves of these organisms often exhibit a complex shape, with episodic cessations or accelerations of growth occurring long after maturation. The mixed allocation to growth and reproduction has poorly understood adaptive consequences, and the life‐history theory does not explain if complex growth in short‐lived organisms can be adaptive.We model the trade‐off between growth and reproduction in a short‐lived organism evolving in a metapopulation. Individuals occupy risky or safe sites throughout their lives, but are uncertain regarding the risk of death. Modelled organisms are allowed to grow and produce offspring at specified time points (moults), although we also consider scenarios that approximate continuous growth and reproduction.Certain combinations of risky to safe sites select for strategies with mixed allocation to growth and reproduction that bet‐hedge offspring production in safe and risky sites. Our model shows that spatially heterogeneous environments select for mixed allocation only if safe sites do not become the prevailing source of recruits, for example, when risky sites are frequent. In certain conditions, growth curves are multi‐phasic, with allocation to growth that stops, remains constant or accelerates during adult life. The resulting complex growth curves are more likely to evolve in short‐lived organisms that moult several times per adult life.Our work shows that spatial heterogeneity can select for growth that accompanies reproduction and provides insights into the adaptive significance of complex growth curves. Short‐lived crustaceans are particularly predisposed to exhibit complex growth patterns as an adaptive response to spatially heterogeneous environments. Our results suggest that standard statistical growth models assuming adult growth rate to only decelerate over life are not well suited to approximate growth curves of short‐lived crustaceans. A free Plain Language Summary can be found within the Supporting Information of this article. [ABSTRACT FROM AUTHOR]

Abstract: The theory of life‐history evolution investigates how growth‐reproduction trade‐offs drive evolution of body size in uni‐ and multivoltine (one or more generations per year) arthropods. Existing theory does not predict how the length of the feeding season (season length hereafter) affects body size in semivoltine (i.e., juvenile period longer than 1 year) determinate growers and usually ignores that uni‐ and semivoltine arthropods accumulate large reserves to cover costs of diapause and future reproduction. Here, we present how the trade‐offs between growth, storage and reproduction drive evolution of body mass and reproductive strategy in arthropods with determinate growth. Our life‐history model concerns high‐latitude marine copepods living in a strongly seasonal environment. We find that small changes in season length and mortality rate translate into abrupt shifts in lean body mass (a proxy for body size). Body size shifts are caused by a change from multi‐ to uni‐ and semivoltine life cycles with semivoltine life histories selected for in short seasons and only if background mortality is low. Shifts in the number of generations per year do not translate into shifts in the mass of lipid reserves. The model predicts less reserves the shorter the winter. Season length alone is not a sufficient predictor of the degree of capital breeding. Storing for reproduction is strongly selected for under short season but low mortality rate. Hence, capital breeding contributes to fitness in uni‐ and semivoltine organisms whereas multivoltines are income breeders. We also show that storing reserves for diapause and capital breeding trades off with adult size of determinately growing arthropods. Our results, in particular regarding optimal body size, reproductive strategy (income‐to‐capital breeding) and degree of storage are relevant to a number of determinate growers, including insects and crustaceans. A plain language summary is available for this article. [ABSTRACT FROM AUTHOR]