Evolutionary significance of phenotypic accommodation in novel environments: an empirical test of the Baldwin effect

Abstract

When faced with changing environments, organisms rapidly mount physiological and behavioural responses, accommodating new environmental inputs in their functioning. The ubiquity of this process contrasts with our ignorance of its evolutionary significance: whereas within-generation accommodation of novel external inputs has clear fitness consequences, current evolutionary theory cannot easily link functional importance and inheritance of novel accommodations. One hundred and twelve years ago, J. M. Baldwin, H. F. Osborn and C. L. Morgan proposed a process (later termed the Baldwin effect) by which non-heritable developmental accommodation of novel inputs, which makes an organism fit in its current environment, can become internalized in a lineage and affect the course of evolution. The defining features of this process are initial overproduction of random (with respect to fitness) developmental variation, followed by within-generation accommodation of a subset of this variation by developmental or functional systems (‘organic selection’), ensuring the organism's fit and survival. Subsequent natural selection sorts among resultant developmental variants, which, if recurrent and consistently favoured, can be inherited when existing genetic variance includes developmental components of individual modifications or when the ability to accommodate novel inputs is itself heritable. Here, I show that this process is consistent with the origin of novel adaptations during colonization of North America by the house finch. The induction of developmental variation by novel environments of this species's expanding range was followed by homeostatic channelling, phenotypic accommodation and directional cross-generational transfer of a subset of induced developmental outcomes favoured by natural selection. These results emphasize three principal points. First, contemporary novel adaptations result mostly from reorganization of existing structures that shape newly expressed variation, giving natural selection an appearance of a creative force. Second, evolutionary innovations and maintenance of adaptations are different processes. Third, both the Baldwin and parental effects are probably a transient state in an evolutionary cycle connecting initial phenotypic retention of adaptive changes and their eventual genetic determination and, thus, the origin of adaptation and evolutionary change.