Can extreme climatic events induce shifts in adaptive potential? A conceptual framework and empirical test with Anolis lizards.

Multivariate adaptation to climatic shifts may be limited by trait integration that causes genetic variation to be low in the direction of selection. However, strong episodes of selection induced by extreme climatic pressures may facilitate future population-wide responses if selection reduces trait integration and increases adaptive potential (i.e., evolvability). We explain this counter-intuitive framework for extreme climatic events in which directional selection leads to increased evolvability and exemplify its use in a case study. We tested this hypothesis in two populations of the lizard Anolis scriptus that experienced hurricane-induced selection on limb traits. We surveyed populations immediately before and after the hurricane as well as the offspring of post-hurricane survivors, allowing us to estimate both selection and response to selection on key functional traits: forelimb length, hindlimb length, and toepad area. The direct selection was parallel in both islands and strong in several limb traits. Even though overall limb integration did not change after the hurricane, both populations showed a non-significant tendency toward increased evolvability after the hurricane despite the direction of selection not being aligned with the axis of most variance (i.e., body size). The population with comparably lower between-limb integration showed a less constrained response to selection. Hurricane-induced selection, not aligned with the pattern of high trait correlations, likely conflicts with selection occurring during normal ecological conditions that favours functional coordination between limb traits, and would likely need to be very strong and more persistent to elicit a greater change in trait integration and evolvability. Future tests of this hypothesis should use G-matrices in a variety of wild organisms experiencing selection due to extreme climatic events.

Development and function explain the modular evolution of phalanges in gecko lizards.

Selective regimes favouring the evolution of functional specialization probably affect covariation among phenotypic traits. Phalanges of most tetrapods develop from a conserved module that constrains their relative proportions. In geckos, however, biomechanical specializations associated with adhesive toepads involve morphological variation in the autopodium and might reorganize such modular structures. We tested two hypotheses to explain the modular architecture of hand bones in geckos, one based on developmental interactions and another incorporating functional associations related to locomotion, and compared the empirical support for each hypothetical module between padded and padless lineages. We found strong evidence for developmental modules in most species, which probably reflects embryological constraints during phalangeal formation. Although padded geckos exhibit a functional specialization involving the hyperextension of the distal phalanges that is absent in padless species, the padless species are the ones that show a distal functional module with high integration. Some ancestrally padless geckos apparently deviate from developmental predictions and present a relatively weak developmental module of phalanges and a strongly integrated distal module, which may reflect selective regimes involving incipient frictional adhesion in digit morphology. Modularity of digit elements seems dynamic along the evolutionary history of geckos, being associated with the presence/absence of adhesive toepads.

Correlational selection in the age of genomics.

Ecologists and evolutionary biologists are well aware that natural and sexual selection do not operate on traits in isolation, but instead act on combinations of traits. This long-recognized and pervasive phenomenon is known as multivariate selection, or-in the particular case where it favours correlations between interacting traits-correlational selection. Despite broad acknowledgement of correlational selection, the relevant theory has often been overlooked in genomic research. Here, we discuss theory and empirical findings from ecological, quantitative genetic and genomic research, linking key insights from different fields. Correlational selection can operate on both discrete trait combinations and quantitative characters, with profound implications for genomic architecture, linkage, pleiotropy, evolvability, modularity, phenotypic integration and phenotypic plasticity. We synthesize current knowledge and discuss promising research approaches that will enable us to understand how correlational selection shapes genomic architecture, thereby linking quantitative genetic approaches with emerging genomic methods. We suggest that research on correlational selection has great potential to integrate multiple fields in evolutionary biology, including developmental and functional biology, ecology, quantitative genetics, phenotypic polymorphisms, hybrid zones and speciation processes.

Copulatory function and development shape modular architecture of genitalia differently in males and females.

Genitalia are multitasking structures whose development is mediated by numerous regulatory pathways. This multifactorial nature provides an avenue for multiple sources of selection. As a result, genitalia tend to evolve as modular systems comprising semi-independent subsets of structures, yet the processes that give rise to those patterns are still poorly understood. Here, we ask what are the relative roles of development and function in shaping modular patterns of genitalia within populations and across species of stink-bugs. We found that male genitalia are less integrated, more modular, and primarily shaped by functional demands. In contrast, females show higher integration, lower modularity, and a predominant role of developmental processes. Further, interactions among parts of each sex are more determinant to modularity than those between the sexes, and patterns of modularity are equivalent between and within species. Our results strongly indicate that genitalia have been subjected to sex-specific selection, although male and female genitalia are homologous and functionally associated. Moreover, modular patterns are seemingly constant in the evolutionary history of stink-bugs, suggesting a scenario of multivariate stabilizing selection within each sex. Our study demonstrates that interactions among genital parts of the same sex may be more fundamental to genital evolution than previously thought.