Canalization and adaptation in a landscape of sources and sinks

Abstract

Landscapes are often spatially heterogeneous, and many species frequently confront novel environments to which they are not adapted. Whether a species becomes adapted to a novel environment, and thus undergoes niche evolution, may depend not only on the genetic architecture of the traits under selection, but also on the structure of the ecological landscape. Different models of gene architecture are used to show that complex genetic architectures tends to produce genetic canalization that slows adaptation to novel environments compared to simpler additive polygenic architectures, but that the topology of the landscape interacts with genetic architecture to influence the probability of adaptation. This interaction can lead to unexpected results, such as a greater probability of adaptation to a novel environment for a population of more highly canalized individuals than a population of less canalized individuals. The interplay between landscape structure and genetic architecture may influence the balance of evolutionary forces acting on a population, and thus whether a species is likely to adapt to the novel environments it confronts.

Theoretical Perspectives on the Statics and Dynamics of Species’ Borders in Patchy Environments

“…The reason is that the interplay of selection and gene flow within populations alters the entire distributions of genotypes available for sampling by emigration and may increase the number of individuals found in a fattened tail, who are incidentally more likely to be able to found populations outside the range of habitats already occupied by the species. In general, the details of genetic architecture and the magnitude of the phenotypic effect of likely mutations appear to matter greatly in range dynamics (Kawecki 2000, 2008; Gomulkiewicz et al 2010; Kimbrell 2010; Turner and Wong 2010). This is particularly likely if adaptive evolution permitting persistence requires adaptation to multiple distinct ecological factors, where genetic correlations can constrain evolution (Blows and Hoffmann 2004; Hellmann and Pineda-Krch 2007; Gomulkiewicz and Houle 2009; Walsh and Blows 2009).…”

Landscape structure and genetic architecture jointly impact rates of niche evolution

“…While this study is one of the first to investigate the dynamics of niche evolution and range expansion in complex, continuous landscapes, a number of additional factors that potentially influence rates of adaptation remain to be tested. For example, epistatic and pleiotropic effects can interact with the spatial constellation of habitat in a system of several interconnected patches to affect evolutionary outcomes (Kimbrell ). In these cases, complex genetic architectures often lead to genetic canalization, which might hamper adaptation to new environments (Kimbrell ).…”

“…For example, epistatic and pleiotropic effects can interact with the spatial constellation of habitat in a system of several interconnected patches to affect evolutionary outcomes (Kimbrell ). In these cases, complex genetic architectures often lead to genetic canalization, which might hamper adaptation to new environments (Kimbrell ). Also, linkage might modulate adaptive dynamics as selection tends to create positive linkage disequilibrium between beneficial alleles, resulting in larger genetic variation and a greater response to selection (Kawecki ).…”

“…In addition to landscape structure, the genetic architecture of traits under selection may influence the likelihood and rate of adaptation to novel conditions (Kawecki , , Kimbrell and Holt , Gomulkiewicz et al , Kimbrell ). A so far unresolved question is whether adaptation in polygenic traits (which typically are believed to be those involved in adaptation to marginal environments) is more likely to arise as a result of many mutations of small phenotypic effects or as a result of a few large mutations (Orr ).…”

Selection for distinct gene expression properties favours the evolution of mutational robustness in gene regulatory networks

“…The model of gene regulatory networks that I employ has allowed addressing important topics in evolutionary biology (Fierst & Phillips, ). Such topics include the relationship between sexual reproduction and epistasis (Azevedo et al ., ; MacCarthy & Bergman, ; Martin & Wagner, ; Lohaus et al ., ), how network structure affects evolution (Siegal et al ., ; Espinosa‐Soto & Wagner, ; Pinho et al ., ), the evolution of evolvability (Ciliberti et al ., ; Kimbrell & Holt, ; Draghi & Wagner, ; Kimbrell, ; Whitacre & Bender, ; Espinosa‐Soto et al ., ; Fierst, ; Steiner, ), the effects of phenotypic plasticity on evolution (Masel, ; Espinosa‐Soto et al ., , b; Fierst, ; Pinho et al ., ), how hybrid incompatibility evolves (Palmer & Feldman, ; Le Cunff & Pakdaman, ) and even the role of gene network dynamics in the evolution of organismal complexity (Lohaus et al ., ). Importantly, the model has been rewarding when used to investigate how mutational robustness evolves (Wagner, ; Siegal & Bergman, ; Bergman & Siegal, ; Ciliberti et al ., ; Huerta‐Sánchez & Durrett, ; Kimbrell, ; Le Cunff & Pakdaman, , ; Fierst, ).…”