AN INTRODUCTION TO THE BALDWIN EFFECT
James Mark Baldwin (1861–1934) was an American psychologist who devised two concepts, “organic selection” and “orthoplasy,” now commonly known as the “Baldwin effect” (term coined by Simpson 1953). Baldwin's theory is based on the principle that individuals are plastic and able to adapt to their environment within a generation. This plasticity dictates which individuals will survive and produce offspring and thus dictates the course of evolution. By no means, however, did he believe that acquired phenotypes could be inherited. On the contrary, he believed that natural selection acts on “variations in the direction of the plasticity…” (Baldwin 1902, p. 37). He thus proposed that plasticity would be a positive driving force of evolution, setting the stage for further neo-Darwinian evolution by increasing the survival of those who display a plastic response. Over time, standing genetic variation can be selected upon so that evolution can proceed in the direction of the induced plastic response. He referred to the ability of plasticity to increase survival as “organic selection,” and the directional influence of organic selection on evolution as “orthoplasy” (Baldwin 1896, 1902). Because Baldwin was a psychologist, he focused heavily on the role of plasticity in behavior and learning, that is labile traits, yet also recognized that plasticity occurs in other aspects of the phenotype as well. His theories can be broadly applied, and can include developmentally plastic, nonlabile traits.
Baldwin often spoke of “accommodation” in reference to nonheritable phenotypic changes that occur in response to the environment and increase the survival of the organism in the particular environment in which the phenotype is induced (Baldwin 1896, 1902). The term “accommodation” is still used for similar effects today, although we now divide accommodation into genetic and phenotypic components (West-Eberhard 2003, 2005; Braendle and Flatt 2006). “Phenotypic accommodation” (West-Eberhard 2003, 2005) is the modern-day equivalent of Baldwin's “accommodation,” except that the modern term incorporates responses to both genetic innovations and environmentally induced changes, whereas Baldwin used the term to only refer to the latter. “Genetic accommodation” (West-Eberhard 2003) is a similar concept related to adaptive genetic changes and will be discussed below. West-Eberhard (2005) defines phenotypic accommodation as “adaptive mutual adjustment, without genetic change, among variable aspects of the phenotype, following a novel or unusual input [genetic or environmental] during development.” Another difference between Baldwin's and West-Eberhard's definitions is that Baldwin's may also include labile (i.e., nondevelopmental) plastic changes. An example of phenotypic accommodation is the “two-legged goat effect,” detailed in West-Eberhard (2003, 2005). A mutant goat was born in the early 1900s, without functional forelimbs (Slijper 1942a,b; West-Eberhard 2003, 2005). We can here think of the absence of functional forelimbs as an environment to which the goat must subsequently respond. Through development, this goat was able to adopt bipedal locomotion via enlargement of the hind legs and changes to the spine and pelvis (i.e., a plastic response). Similar phenomena were observed in baboons (Papio ursinus; reviewed by West-Eberhard 2003) and Japanese macaques (Macaca fuscata; Hirasaki et al. 2004).
Baldwin noted that heritable variation can occur in the same direction as the plastic response (which he termed “coincident variations”), and thus phenotypes that are originally environmentally induced can be selected upon and inherited (Baldwin 1902). Currently, this phenomenon is considered a type of “genetic accommodation” and empirical examples have been documented (see examples below). In her definition of genetic accommodation, West-Eberhard (2003, p. 142) includes “gene-frequency change due to selection on the regulation, form, or side effects of a novel trait.” Although Baldwin emphasized that evolution would occur in response to an environmentally induced novel trait, “genetic accommodation” is now commonly used to refer to evolution in response to both genetically based and environmentally induced novel traits (Table 1).
Table 1. Mechanisms of evolutionary change mediated by phenotypic plasticity, and characteristics inherent to each mechanism.
|Baldwin effect||environmental||neither or increase1||changes|
|genetic assimilation||environmental||decrease||stays the same|
|genetic accommodation||environmental or genetic||neither or either||changes or stays the same2|
Another type of genetic accommodation is “genetic compensation” (Grether 2005). Here, the environmentally induced phenotype is maladaptive, and selection favors genetic variation that occurs in a different direction than the plastic response (i.e., countergradient variation; Conover and Schultz 1995), so that a genetic change compensates for the plastic change. The end result may be an increase or decrease in plasticity, or no change in the level of plasticity. Because maladaptive plasticity was not considered in Baldwin's theory, I will not discuss genetic compensation in detail.
Baldwin maintained that both neo-Darwinism and neo-Lamarckism were inherently deficient in explaining evolution. His two criticisms of neo-Darwinism were (1) small genetic variations in the “lines of progress” were not substantial enough to adapt an organism to its environmental conditions, and (2) when structure and function of complex traits were only partially correlated, as in the early evolution of these traits, their utility would be of little advantage (Baldwin 1902). Baldwin posited that environmental induction, or accommodation, could enhance such variation or correlations. He did note, however, that neo-Darwinian natural selection is a requirement for evolution to occur after a plastic response to a novel environmental stimulus (Baldwin 1902). He criticized neo-Lamarckism more severely, stating that little or no evidence for the inheritance of acquired characters exists, and that the theory is purely speculative.
Examples of Baldwin's organic selection can be observed in nature. Yeh and Price (2004) examined dark-eyed juncos (Junco hyemalis) from California. In the early 1980s, individuals from an ancestral mountain population colonized and established a coastal population. The coastal environment is milder, with less seasonal variation. Yeh and Price found that the newly colonized coastal population had a breeding season (a highly plastic trait) that was nearly twice as long, and noted that this increase in breeding time was adaptive. They speculate that plasticity facilitated colonization and establishment of the new population. An example of both organic selection and orthoplasy comes from Arctic charr (Salvelinus alpinus) populations from a Scottish lake (Adams and Huntingford 2004). Three different morphs occur sympatrically: a benthivorous morph that feeds on macro-invertebrates, a planktivorous morph, and a piscivorous morph. The head anatomy of these morphs differs to reflect their preferred prey type. Juveniles of the benthivorous and planktivorous morphs were raised in the laboratory in a common-garden environment, and measurements of head size and shape were made on both wild-caught adults and mature laboratory-raised fish. Both genetic and environmental components of morph divergence were observed, suggesting that phenotypic plasticity may have permitted diversification of morphs into their respective niches, hence setting the stage for further genetic diversification.
We can suppose that Baldwin's orthoplasy would be favored if plasticity is limited. In certain cases, a plastic response to a new environment may be adaptive, yet a more extreme phenotypic value would be required to attain maximum fitness. We can imagine a fitness landscape in which an environmentally induced trait pushes an individual up a new fitness peak, but does not allow it to reach the fitness maxima (figure 1 in Price et al. 2003; figure 2 in Ghalambor et al. 2007). In this scenario, positive selection would occur on heritable variation in the direction of the plastic response. Baldwin makes this apparent when he writes,
[m]any functions may be passably performed through accommodation, supplementing congenital [heritable] characters, which would be better performed were the congenital characters strengthened [i.e., if further phenotypic change occurred]. Congenital variation would in these cases by seizing upon this additional utility [plasticity], carry evolution on farther than it had gone before [i.e., result in heritable changes in form]… this would give the gradual shifting of the congenital mean toward the full endowment [phenotypic optimum]… (Baldwin 1902, pp. 209–210)
Other such limits identified by DeWitt et al. (1998) include unreliable environmental cues and lag time between sensing an environmental cue and production of the appropriate phenotype. An empirical example of shifts in the mean phenotypic value without a change in the level of plasticity is documented in a cichlid fish (Pseudocrenilabrus multicolor) from low-oxygen swamps and well-oxygenated rivers and lakes in Uganda. Chapman et al. (2000, L. Chapman et al., unpubl. ms.) found that aspects of gill size were greater in swamp fish than in lake fish, and similar patterns were observed when fish were raised under high or low oxygen treatments in the laboratory. Further analyses revealed that levels of plasticity were not significantly different among populations, although populations differed in their mean gill size when raised under common conditions (L. Chapman et al., unpubl. ms.). These results indicate that since the time of population divergence, genetic accommodation has resulted in mean differences in gill size among populations, even though the ability of the gills to respond to environmental cues has remained constant. Similar results were found by Van Buskirk and Arioli (2005) in tadpoles (Rana temporaria) raised with or without predators. Tadpoles exhibited plasticity in predator avoidance behavior, as well as behavioral differences among populations, yet behavioral plasticity did not differ among populations. These results suggest that phenotypic values across environments can evolve independently of the level of plasticity.
Baldwin (1902, pp. 36–37) also proposed that plasticity itself could be adaptive and selected for, thus increasing plasticity in a population. Recent interest in this theory has resulted in empirical support confirming Baldwin's intuition (e.g., Gianoli and González-Teuber 2005; Nussey et al. 2005; Richter-Boix et al. 2006). It is intuitive that plasticity should often increase under selection, if the most plastic individuals are the most capable of colonizing a novel environment or persisting in a fluctuating environment. In these instances, the individuals with the highest levels of plasticity would be under positive selection. Via (1993a,b) argues that plasticity itself would not be selected upon, but rather subject to indirect selection via selection on the most extreme trait values representing the upper limits of the plastic response. Scheiner and Lyman (1989) and Schlichting and Pigliucci (1993) on the other hand, propose that selection can occur directly on plasticity, if plasticity increases the matching between the environmental conditions and the corresponding optimal phenotype. Although these two views of selection on plasticity differ, the outcome of both cases is identical: plasticity will increase due to selection, regardless of whether selection acts on the level of plasticity or on the induced traits/trait values. Indeed, Richard Wolterek (1909), inventor of the term “reaktionsnorm” (i.e., reaction norm), proposed that the reaction norm, rather than the trait value, is inherited because nearly all traits are plastic under at least some environmental conditions (reviewed by Sarkar 2004).
Several empirical examples indicate that plasticity increases after selection under new environmental conditions. For example, Parsons and Robinson (2006) found that the body shape of pumpkinseed sunfish (Lepomis gibbosus) was more plastic in the derived open-water ecomorph than in the ancestral inshore ecomorph, even though the habitat of the latter is more heterogeneous. Similarly, Aubret et al. (2004) found that the head and jaw length of tiger snakes (Notechis scutatus) were plastic in island populations that feed on large prey, but were not plastic in mainland populations that feed on small prey. Presumably, island populations were colonized from the mainland, and plasticity allowed snakes to exploit the new prey source. Even Waddington (1959) found that plasticity can increase after episodes of directional selection (discussed below).
In summary, the Baldwin effect allows for adaptive evolution through adaptive phenotypic plasticity, which improves fitness, thus dictating the course of future neo-Darwinian evolution. West-Eberhard (2003, p. 153) states that the Baldwin effect is a type of genetic accommodation in which only changes in the regulation of a trait (i.e., decreased genetic control, or rather increased plasticity) occur. However, Baldwin clearly indicated that not only the regulation, but also the form of a trait could change as an evolutionary response to a new environmental stimulus (see above). Genetic assimilation is another type of genetic accommodation also relying upon environmental induction, but this mechanism relies only on evolutionary change in the regulation of a novel trait and on its frequency of occurrence in a population (Hall 2001; West-Eberhard 2003, 2005).