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Abstract Coevolution has come to be widely understood as specific, simultaneous, reciprocal adaptation by pairs of interacting species. This strict-sense definition arose from a desire for conceptual clarity, but it has never reflected the much wider diversity of ways in which interacting species may shape each other’s evolution. As a result, much of the literature on the evolutionary consequences of species interactions pays homage to the strict-sense definition while addressing some other form of coevolution. This tension suggests we should reframe the key question in coevolution research, from “when is it coevolution?” to, rather, “how is it coevolution?”. The result is not so much a definition of coevolution as a mission statement: We can describe how species coevolve by documenting the ways that each species shaped the other’s genetic diversity over a shared history of interaction. Making this change shifts our focus from identifying case studies for a single, narrowly defined process to describing the many ways—specific and diffuse, simultaneous and stepwise, and adaptive and nonadaptive—in which species evolve together. 

Abstract Phenotypic expression is often constrained by functional conflicts between traits, and the resulting trade-offs impose limits on phenotypic and taxonomic diversity. However, the underlying mechanisms that maintain trade-offs or allow organisms to resolve them via phenotypic plasticity are often challenging to detect. The trade-off between gas exchange and water loss across respiratory surfaces represents a fundamental trade-off that constrains phenotypic diversity in terrestrial life. Here, we investigate plastic mechanisms that mitigate this trade-off in lungless salamanders that breathe exclusively across their skin. Our field and laboratory experiments identified plastic responses to environmental variation in water loss and oxygen uptake, and gene expression analyses identified putative pathways that regulate this trade-off. Although the trade-off was generally strong, its strength covaried with environmental conditions. At the molecular level, antagonistic pleiotropy in multiple biological pathways (e.g., vasoconstriction and upregulation of aerobic respiration) putatively produce the trade-off, while other pathways mitigate the trade-off by affecting a single trait (e.g., oxygen binding affinity, melanin synthesis). However, organisms are likely to encounter novel trade-offs in the process of bypassing another. Our study provides evidence that alternative pathways allow organisms to mitigate pleiotropic conflicts, which ultimately may allow greater phenotypic diversity and persistence in novel environments. 

Abstract Abiotic and biotic factors interact to influence phenotypic evolution; however, identifying the causal agents of selection that drive the evolution and expression of traits remains challenging. In a field common garden, we manipulated water availability and herbivore abundance across 3 years, and evaluated clinal variation in functional traits and phenology, phenotypic plasticity, local adaptation, and selection using diverse accessions of the perennial forb, Boechera stricta. Consistent with expectations, drought stress exacerbated damage from herbivores. We found significant plasticity and genetic clines in foliar and phenological traits. Water availability and herbivory interacted to exert selection, even on traits like flowering duration, which showed no clinal variation. Furthermore, the direction of selection on specific leaf area in response to water availability mirrored the genetic cline and plasticity, suggesting that variation in water levels across the landscape influences the evolution of this trait. Finally, both herbivory and water availability likely contribute to local adaptation. This work emphasizes the additive and synergistic roles of abiotic and biotic factors in shaping phenotypic variation across environmental gradients. 

Abstract Phenotypic plasticity can alter traits that are crucial to population establishment in a new environment before adaptation can occur. How often phenotypic plasticity enables subsequent adaptive evolution is unknown, and examples of the phenomenon are limited. We investigated the hypothesis of plasticity-mediated persistence as a means of colonization of agricultural fields in one of the world’s worst weeds, Raphanus raphanistrum ssp. raphanistrum. Using non-weedy native populations of the same species and subspecies as a comparison, we tested for plasticity-mediated persistence in a growth chamber reciprocal transplant experiment. We identified traits with genetic differentiation between the weedy and native ecotypes as well as phenotypic plasticity between growth chamber environments. We found that most traits were both plastic and differentiated between ecotypes, with the majority plastic and differentiated in the same direction. This suggests that phenotypic plasticity may have enabled radish populations to colonize and then adapt to novel agricultural environments. 

Abstract Island biotas provide unparalleled opportunities to examine evolutionary processes. Founder effects and bottlenecks, e.g., typically decrease genetic diversity in island populations, while selection for reduced dispersal can increase population structure. Given that support for these generalities mostly comes from single-species analyses, assemblage-level comparisons are needed to clarify how (i) colonization affects the gene pools of interacting insular organisms, and (ii) patterns of genetic differentiation vary within assemblages of organisms. Here, we use genome-wide sequence data from ultraconserved elements (UCEs) to compare the genetic diversity and population structure of mainland and island populations of nine ant species in coastal southern California. As expected, island populations (from Santa Cruz Island) had lower expected heterozygosity and Watterson’s theta compared to mainland populations (from the Lompoc Valley). Island populations, however, exhibited smaller genetic distances among samples, indicating less population subdivision. Within the focal assemblage, pairwise Fst values revealed pronounced interspecific variation in mainland-island differentiation, which increases with gyne body size. Our results reveal population differences across an assemblage of interacting species and illuminate general patterns of insularization in ants. Compared to single-species studies, our analysis of nine conspecific population pairs from the same island-mainland system offers a powerful approach to studying fundamental evolutionary processes. 

Abstract The genetic dissection of reproductive barriers between diverging lineages provides enticing clues into the origin of species. One strategy uses linkage analysis in experimental crosses to identify genomic locations involved in phenotypes that mediate reproductive isolation. A second framework searches for genomic regions that show reduced rates of exchange across natural hybrid zones. It is often assumed that these approaches will point to the same loci, but this assumption is rarely tested. In this perspective, we discuss the factors that determine whether loci connected to postzygotic reproductive barriers in the laboratory are inferred to reduce gene flow in nature. We synthesize data on the genetics of postzygotic isolation in house mice, one of the most intensively studied systems in speciation genetics. In a rare empirical comparison, we measure the correspondence of loci tied to postzygotic barriers via genetic mapping in the laboratory and loci at which gene flow is inhibited across a natural hybrid zone. We find no evidence that the two sets of loci overlap beyond what is expected by chance. In light of these results, we recommend avenues for empirical and theoretical research to resolve the potential incongruence between the two predominant strategies for understanding the genetics of speciation. 

Abstract The theory describing the evolution of offspring size often assumes that the production cost per unit volume is the same for small and large offspring. However, this may not be true if indirect costs of reproduction (e.g., material and energetic costs of supporting offspring development) scale disproportionately with offspring size. Here we show how direct and indirect costs of reproduction can be explicitly modeled within the Smith–Fretwell framework and how observations of size-number relationships can thus be used to evaluate indirect costs. We applied this analysis to measures of egg volume and fecundity for over 300 individuals of a coastal fish species and found that the tradeoff was much stronger than the expected inverse (fecundity scaled with volume−1.843). Larger offspring were thus more expensive to produce. For our study species, an important indirect cost was that larger eggs were accompanied by disproportionately more ovarian fluid. Calorimetry and removal experiments were used to further measure both the energetic costs and fitness benefits of ovarian fluid. In addition, we show that indirect costs of reproduction can intensify size-number tradeoffs in a variety of fishes. Indirect costs of reproduction can be large and may therefore play an important role in the evolution of offspring size.