JOURNAL OF EXPERIMENTAL ZOOLOGY (MOL DEV EVOL) 304B:610-618 (2005) Phenotypic Accommodation: Adaptive Innovation Due to Developmental Plasticity MARY JANE WEST-EBERHARD* Smithsonian Tropical Research Institute, Escuela de Biologia, Universidad de Costa Rica, Costa Rica, Centroamerica ABSTRACT Phenotypic accommodation is adaptive adjustment, without genetic change, of variable aspects of the phenotype following a novel input during development. Phenotypic accommodation can facilitate the evolution of novel morphology by alleviating the negative effects of change, and by giving a head start to adaptive evolution in a new direction. Whether induced by a mutation or a novel environmental factor, innovative morphological form comes from ancestral developmental responses, not from the novel inducing factor itself. Phenotypic accommodation is the result of adaptive developmental responses, so the novel morphologies that result are not "random" variants, but to some degree reflect past functionality. Phenotypic accommodation is the first step in a process of Darwinian adaptive evolution, or evolution by natural selection, where fitness differences among genetically variable developmental variants cause phenotype-frequency change due to gene- frequency change. J. Exp. Zool. (Mol. Dev. Evol.) 304B.-610-618, 2005. © 2005 Wiley-Liss, Inc. Adaptive responsiveness to conditions in the ties; Goldschmidt ('40 ['82]), who discussed how external and internal environment has long been the "regulative ability" of developmental mechan- considered a universal property of living things. isms could facilitate and exaggerate change; Large subdisciplines of the biological sciences, Frazzetta ('75), who referred to phenotypic "com- including physiology, endocrinology, neurobiology, pensation"; Muller ('90) on "ontogenetic buffer- ethology, embryology, cell biology, and the mole- ing"; and Kirschner ('92); and Gerhart and cular biology of gene expression, study the Kirschner ('97), who consider the mechanisms of mechanisms of adaptive responsiveness, but its phenotypic accommodation within cells and dur- significance for the process of evolution has not ing embryogenesis an aspect of "evolvability." been extensively explored. Elsewhere I have argued that developmental PHENOTYPIC ACCOMMODATION IN plasticity, or responsiveness to external and inter- MORPHOLOGY: THE TWO-LEGGED-GOAT nal environments whether adaptive or not, can play EFFECT an important role in evolution (West-Eberhard, 2003). Here I summarize one aspect of that Phenotypic accommodation can include adap- argument, namely, that adaptive flexibility, or tive plasticity in all aspects of the phenotype, phenotypic accommodation, can facilitate the origin including not only morphology, but also physiol- and evolution of morphological novelties. Phenoty- ogy and behavior. And it can involve developmen- pic accommodation is adaptive mutual adjustment, tal plasticity at more than one level of without genetic change, among variable aspects of organization. For example, behavioral accommo- the phenotype, following a novel or unusual input dation may involve flexible responses of many during development (West-Eberhard, '98, 2003). organs (e.g., heart, brain, and limbs) and mechan- The role of flexibility in facilitating evolutionary isms that operate at multiple levels within change has been noted by many authors, including them (i.e., tissues, cells, and their component most prominently Baldwin (1896, '02), whose concept of "organic selection" meant fitness enhancement due to phenotypic accommodation; Correspondence to: Mary Jane West-Eberhard, Escuela de Biologia, Universidad de Costa Rica, Costa Rica, Centroamerica. Schmalhausen ('49 ['86]), who saw individual E-mail: [email protected] Received 25 November 2004; Accepted 15 July 2005 adaptability as a stabilizing force that promotes Published online 13 September 2005 in Wiley InterScience the origin and evolution of morphological novel- (www.interscience.wiley.com). DOI: 10.1002/jez.b.21071. 2005 WILEY-LISS, INC. PHENOTYPIC ACCOMMODATION 611 organelles) (see West-Eberhard, 2003). There are rise to it." Muller and Wagner ('91, p 243) define subdisciplines of biology that deal with adaptive morphological novelty as "a structure that is accommodation in physiology and behavior, but neither homologous to any structure in the there is no comparable field devoted primarily to ancestral species nor homonomous to any other adaptive responses in morphology. Adaptive mor- structure of the same organism." But this defini- phological plasticity is nonetheless well documen- tion is impossible to apply given the reorganiza- ted, for example in studies of vertebrate muscle tional nature of evolutionary change. Unless and bone (reviews in Slijper, '42a, b; Frazzetta, "homologous" means identical, many novelties '75; Wimberger, '94); invertebrate body size and must have recognizable homologs in ancestral form (e.g., see Bernays, '86; Strathmann et al., species which have given rise to them through '92); and in plants, perhaps the best studied group ontogenetic repatterning (Wake and Roth, '89; of organisms with respect to morphological plas- developmental recombination of West-Eberhard, ticity (reviews in Bradshaw, '65; Schlichting, '86; 2003, 2005). Some innovations, such as those Sultan, '87, 2000). derived via heterotopy (change in the location of A handicapped goat studied by Slijper ('42a, b) expression of an ancestral trait), may exist along- can serve to illustrate the phenomenon of mor- side the ancestral morphology as homonymous phological phenotypic accommodation. Slijper's structures in the descendent species. [For a more goat was born with congenital paralysis of its extensive discussion of the homology concept as front legs, so that it could not walk on all fours. It related to developmental plasticity and evolution, managed to get around by hopping on its hind see West-Eberhard (2003) and references therein.] legs, an example of behavioral accommodation The two-legged goat is an instructive example that led to dramatic morphological accommoda- for anyone interested in morphological innovation. tion as well. When the goat died an accidental It does not matter, for the form taken by the death at the age of 1 year, Slijper dissected it and morphological change, whether the pivotal change published a description of its altered morphology, (inability to walk on the front legs) was induced by which included changes in the bones of the hind a mutation or by an environmental accident. The legs, the shape of the thoracic skeleton and particular characteristics of the novel morphology, sternum, changes in the shape and strength of that is, the novel features of the bones, muscles the pelvis, which developed an unusually long and tendons, arose via mechanisms of develop- ischium. Changes in the pelvic muscles included a mental plasticity, not owing to the particular greatly elongated and thickened gluteal tongue genetic or environmental change that may have whose attachment to the bone was reinforced by a induced them. Any number of mutations or novel trait, a set of numerous long, flat tendons. environmental factors could have triggered a This example of phenotype accommodation defect in the front legs. Whatever the trigger, it shows how developmental responses can mold acted as a kind of switch mechanism that the form of a morphological novelty. In Slijper's controlled a whole suite of morphological goat, novel morphology came not from a series of changes—a complex, coordinated morphological mutational changes, but from reorganized expres- novelty, a new modular "trait" whose develop- sion of capacities that were already present. In the mental independence of others is defined by the remainder of this article, I show how such integrated response of the phenotype to a new immediate responses can be converted to evolu- input. tionary change and facilitate the origin of adaptive A second important point is that the morpholo- novelties. gical change was mediated by behavior. Behavior is, of course, a common mediator of normal PHENOTYPIC ACCOMMODATION AND skeletal and muscle development because it is THE ORIGINS OF NOVELTY especially flexible in response to environmental contingencies. It follows that behavior must often A morphological innovation can be defined as an be an important mechanism in the origins of novel aspect of morphology that was not present in the morphological traits. So we have to list behavior immediate ancestors of a species, in a given life and its neuroendocrinological underpinnings, stage and sex. Mayr ('59, p 89) defined an alongside genomic changes, as among the primary evolutionary novelty as "any newly arisen char- developmental causes of morphological novelty. acter, structural or otherwise, that differs more Two-legged goats are unjustly maligned if than quantitatively from the character that gave treated as mere freaks with no evolutionary 612 M.J. WEST-EBERHARD importance. Slijper ('42a, b) compared the mor- for the powerful muscles used in chewing the phology of the two-legged goat with that of other bones and tough meat of the hyenas' prey (after bipedal mammals such as humans and kangaroos. Holekamp and Smale, '98; Holekamp, personal Some of its novel morphological features closely communication). The extreme modifications of the resemble the evolutionary novelties of bipedal head are absent in infants of the same species, and mammals: its compressed thorax and its elongate they also fail to develop in captive individuals fed