ROLE OF DEVELOPMENT IN EVOLUTION

individuals that reproduce and thus evolve. Mutations existing in individu- als would not have any consequences to evolution unless the resulting trait is expressed in populations of similar organisms

(G. C.

Williams,

1966).

Evolution, then, becomes the change in genetic composition within populations.

The modem synthesis’s emphasis on the separation of the somatic and germ line essentially afforded no role for development in evolution.

Development may result from the differential expression of genes in interac- tion with the environment, but such effects are governed directly

by

the genome, and variations in development, brought about by variations in the environment, cannot affect the germ line and thus cannot exert any influence on evolution (see Gottlieb, 1992).

The modern synthesis remains intact today, although evolutionary theory has not stood still. For example, the theorizing of evolutionary biolo- gist William Hamilton (1964) and the concept of inclusive fitness (see chapter

2),

and the theories of evolutionary biologist Robert Trivers (1971, 1972,

1974;

see chapters

8

and

9),

among others, have changed the focus of evolutionary theory. The advent of sociobiology (Dawkins,

1976; E. 0.

Wilson,

1975),

with its emphasis on explaining complex social behavior, such as altruism, in terms of evolutionary principles, focused attention on the evolution of behavior, something that many developmental psychologists found appealing (MacDonald,

1988).

But the basic tenets of the modern synthesis (other than the possibility that evolution is not as gradual as Darwin originally postulated, see discussion of punctuated equilibrium below) have not been seriously questioned, and development has not been given a promi- nent role in evolutionary explication. Evolutionary psychology has been no exception (see Barkow, et al., 1992; Buss,

1999).

with humans at the pinnacle, just below angels in a divine plan (Charles- worth, 1992; Morss, 1990). This was captured

by

the principle of orthogenesis, the belief that there is an inherent perfecting force in all of organic life that makes evolution always moving “forward.” More “advanced” species, such as humans, relative to less advanced species, such as chimpanzees (or more properly, our ape-like ancestors), evolved

by

adding something to the adult stages of ancestors. So, for example, humans evolved “more” brain.

Recapitulation Theory and the Biogenetic Law

This

progressive spirit was captured by German biologist and philoso- pher Emst Haeckel (1835-1919), who applied findings in embryology to evolutionary thinking to postulate the biogenetic law (see Gottlieb, 1992;

S. J.

Gould,

1977;

Mayr,

1982;

Schwartz,

1999,

for historical reviews). The biogenetic law was the basis for recapitulation theory,

which

can be captured

by

the phrase “ontogeny recapitulates phylogeny.” This means that the development of the individual (ontogenetic development) goes through, or repeats, the same sequences as the evolutionary development of the species (phylogenetic development), with evidence of these ancestral stages most clearly seen during embryological development. From this perspective, the entire phylogenetic past of a species can be discerned

by

looking at (primar- ily) embryological development, which is essentially a much speeded-up version of evolutionary history. What is new in evolution is what is added to the end states of ontogeny.

This was an attractive theory, in part because it simplified the study of evolution. Studying old bones or the behavior of extant animals to get clues of ancient ancestors would eventually become unnecessary.

All

that was seemingly needed to understand evolution was a detailed knowledge of embryological development. The data, however, were not always consistent with the theory. For example, the order in which a feature appeared in phylogeny

did

not necessarily follow the same path in ontogeny. The devel- opment of teeth and tongues provides a good example. Teeth are an earlier evolutionary invention than tongues, but they appear later than tongues in the embryological development of present-day mammals (de Beer, 1958).

By the mid-l920s, it was becoming clear that there were just too many exceptions. Although no one doubted that many evolutionary innovations were added to the end states of an ancestor, there were many other paths that were also taken, some involving the retardation of certain aspects of development (Davidson,

1914;

Thomdike, 1913; see also Hinde, 1983).

Further, the notion that behavior at a given point in time is a result of past experiences, both “internal” and “external,” violates a widely held assumption that behavior is a result of a complex contemporaneous transac- tion between individuals and their surroundings (Gottlieb et al., 1998;

Lewontin,

1982).

From this view, individual organisms actively “cause”

behavior; consequently, one’s phenotype is in a constant state of flux. Ontog- eny, then, can be thought of not as a simple product of genotype and the current environment, but as a “first-order Markov process” in which the subsequent behavior depends on the immediately preceding phenotype and genotype (Lewontin, 1982, p.

279).

Neoteny: Evolving

by

Starting Over

In large part as a reaction to the excessive and often erroneous claims of recapitulation theory, several theorists in the early part of the

20th

century proposed that evolution often proceeds

by

taking a step backward, so to speak. Haeckel’s proposal that evolution occurred

by

making additions to the end point of ancestral forms represents one way in which differences in developmental timing can influence the course of phylogeny. Genetic- based differences in developmental timing have been referred to as hetero- chrony (de Beer,

1958;

Gould, 1977; McKinney,

1998, 2000;

Shea,

1989, 2000).

Different systems or parts of an organism can develop at different rates, and these rates may be accelerated (as in the case of recapitulation) or retarded relative to the developmental rates experienced

by

one’s ancestors.

Changes in ontogenetic timing produce different phenotypes, and if these phenotypes are adaptive (or at least not maladaptive), they eventually produce phylogenetic changes (i.e., new species; de Beer, 1958). One type of developmental retardation is neoteny (literally “holding youth”), which refers to the retention into adulthood of ancestral embryonic or youthful stages.

The idea of evolutionary change brought about

by

modifications in ontogenetic rates is attractive to evolutionary biologists. Genetic mutations that produced seemingly small changes in the onset or offset of a develop- mental process (mutations in regulatory as opposed to structural genes) can have cascading effects, yielding substantial changes in a phenotype.

“Evolution

by

heterochrony” presents a more parsimonious approach to phylogenetic change than the multiple-point mutations that are presumably required to produce the same degree of phenotypic change in a species.

Modifications of developmental rates can also result in relatively rapid changes (termed saltations) in a species. Although conventional neo- Darwinian perspectives (and evolutionary psychological perspectives) argue that phylogenetic changes must be gradual, evidence exists in the fossil record for long periods of stability (smis) in a species followed by rapid and substantial change (termed punctuated equilibrium; Eldredge & Gould, 1972).

Heterochronic changes provide a mechanism for such saltations. Natural selection will, of course, act on the heterochronically modified organisms, so the inclusion of such changes to explain patterns of evolutionary change

50 THE ORIGINS OF HUMAN NATURE

does not conflict with the principal tenet of evolutionary biology (i.e., natural selection).

In the early part of the 20th century, evolutionary biologists such as Great Britain’s Gavin de Beer

(1958)

and Walter Garstang

(1922)

and the Netherlands’ Louis Bolk

(1926)

proposed that the driving force of evolution is the change in the timing of ontogeny, with neoteny playing an important role.

Of

the early neoteny theorists, Bolk was most concerned with human evolution. Bolk saw as the primary difference between humans and apes the fetal character of the human body, believing that neoteny (or, using his term, fetalimtion), was the essence of humankind. People are apes who, bodily, have never grown up. Bolk’s claims for human evolution were ex- treme. He proposed that all “essential” features of modern humans were retarded, or neotenous, ignoring the fact that different systems or structures show different rates of development. According to Bolk,

There is no mammal that grows as slowly as man, and not one in which the full development is attained at such a long interval after birth

. . .

What is the essential in Man as an organism? The obvious answer is:

The slow progress of his life’s course. (p. 470)

Bolk went so far as to suggest that “man, in his bodily development, is a primate fetus that has become sexually mature” (p. 470).

Evolutionary theory after the modem synthesis tended to ignore issues of developmental timing as a force in evolution. However, the idea was kept alive by a hearty few scientists (de Beer, 1958;

M. F.

A. Montagu,

1962),

and in

1977

was fully revived in a book titled Ontogeny and Phylogeny

by

evolutionary biologist Stephen Jay Gould. Since that time, many research- ers have viewed heterochrony, and specifically neoteny, as playing an impor- tant role in evolution, particularly human evolution (Hattori, 1998;

A.

Montagu, 1989; Schwartz, 1999; Thomson, 1988; Wesson, 1991). For exam- ple, Wesson (1991) suggested that neoteny seems to be a good strategy for evolutionary innovation, permitting “a new beginning and relatively rapid change as the organism backs up evolutionarily to get a better start” (p.

205).

O n a similar note,

S. J.

Gould

(1977)

stated that

The early stages of ontogeny are a storehouse of potential adaptations, for they contain countless shapes and structures that are lost through later allometries. When development is retarded, a mechanism is pro- vided (via retention of fetal growth rates and proportions) for bringing these features forward to later ontogenetic stages. (p. 375)

One well-known example of the role neoteny plays in development is that of the salamander species Axolotl (see

S. J.

Gould, 1977). As with salamanders in general, they start life in the water as tadpoles and then metamorphose into air-breathing, land-dwelling newts. But under certain conditions, when life in the water is good and looks to stay that way for a

while, the tadpoles will mature sexually and reproduce, still in the larval state. That is, the developmental timing of their reproductive system and their gill-to-lung/water-to-land “systems” are independent, with the repro- ductive system maturing while the organism is still morphologically in the juvenile (larval) state. Some of the offspring may then go through the

“normal” developmental sequence, from tadpoles to salamanders, while their parents remain larva (albeit sexually active ones).

Several contemporary scientists have seriously questioned the still- popular view that Homo sapiem is a neotenous species (Langer,

1998;

McKin- ney,

1998,2000;

Parker & McKinney,

1999;

Shea, 1989,2000). We discuss in greater detail issues related to heterochrony, and specifically neoteny, with respect to human evolution in chapter

4

and with regard to cognitive evolution in chapter

5.

However, despite the controversy about the role that developmental retardation may have played in human evolution, heter- ochrony, including both acceleration and retardation, is viewed as an impor- tant mechanism

by

which differences in rates of ontogeny can affect patterns of phylogeny.

Heterochrony should not be thought of as the cause of human (or any species’) evolution, but rather as a description of how changes in ontogeny can contribute to changes in phylogeny. When growth is retarded, for example, other avenues, lost to faster developing organisms, can be explored.

A

similar argument can be made when development is accelerated. Modified developmental rates thus permit evolutionary innovations rather than cause them.

In

many cases, they may be necessary for evolutionary changes to have occurred, but they are not, per se, sufficient to bring about phylogenetic modifications (cf. Wachs, 2000). The pressures for changing the pace of development must be found in the environment, with heterochrony being a response to some of those pressures.

And

once changes are brought about

by

changes in developmental rates, they are subject to the pressures of natural selection.

Epigenetic Theories of Evolution

Epigenetic principles, such as those advocated

by

the developmental systems perspective favored here, emphasize the continuous interaction of the environment, broadly defined, with the biology of the individual. Genes are never activated in isolation, and how (or whether) a gene is expressed is dependent on a host of interacting factors that vary over time (development).

Epigenetic theories of evolution (e.g.,

Ho,

1998) view a developing organ- ism’s response to environmental changes as a mechanism for phylogenetic change. Natural selection still plays an important role in evolution, but it is the developmental plasticity of an organism that provides the creative force for evolution.

52

T H E ORIGINS OF H U M A N NATURE

The Baldwin Effect

One major contribution of developmental theory to evolutionary for- mulation during the pre-synthesis days concerned the possible transmission of acquired responses to stress via non-Lamarckian routes. This process, referred to as organic selection, was derived independently around the turn of the 20th century

by

comparative psychologist Conway Lloyd Morgan

(1852-1936),

biologist Henry Fairfield Osborn

(1857-1933,

and compara- tive developmental psychologist James Mark Baldwin

(1861-1934).

Baldwin

(1902),

however, seems to have had the better press secretary, and the phenomenon became known as the Baldwin effect (for discussion, see Gott- lieh,

1992;

Waddington,

1975).

Baldwin proposed that when a population of individuals experiences some environmental stress, many in the popula- tion

will

die. Others, however, will be able to cope with the stress. These latter individuals will reproduce and pass on these tendencies to their off- spring. What is novel about Baldwin’s proposal is that the environmental stressors produce new phenotypes, physical or (more likely) behavioral changes in an organism that are transmitted to the next generation.

Al-

though these modifications could not be transmitted directly to progeny via genetics, they could be transmitted socially. These mainly behavioral modifications kept members of the species alive until a genetic variation came about. Organic selection refers to internal forces that stabilize the change in subsequent generations. Eventually, the surviving animals will be subject to an appropriate congenital variation, a term Baldwin (seemingly) used to refer to mutations. From this perspective, evolutionary novelty can first arise as developmental modifications in response to a changing environment that somehow becomes inherited.

Baldwin’s account of evolution emphasized individual differences in the adaptability of organisms. That is, some individuals are more susceptible to modification given a novel environment.

Waddington’s Genetic Assimilation

Baldwin’s idea has always been out of the mainstream of the modem synthesis (as have all developmental explanations) and has often been seen as being Lamarckian or, at best, neo-Lamarckian. There were several difficulties with the theory, the most prominent being the lack of evidence that any such phenomenon exists. Experimental evidence consistent with the Baldwin effect was demonstrated in the

1950s by

the British biologist Conrad

H.

Waddington (all references to Waddington’s work are from his

1975

collection of essays, The Evolution of an Evolutionist).

In

a classic experiment, Waddington exposed pupal fruit flies (Drosophila melanoguster) to heat shock. Some of the surviving flies responded to this treatment by developing wings with few or no cross veins. Waddington then selectively

bred flies without cross veins and exposed the pupa of the next generation to heat shock, which yielded a second generation of flies with few or no cross veins. He continued this procedure for

14

generations, at which time some of the flies developed the no-cross-veined-wing phenotype without being exposed to the heat shock. That is, a new phenotype,

which

was initially elicited only

by

exposure to an extreme environment (that killed many of those exposed), was eventually displayed spontaneously

by

offspring of no-cross-veined-winged parents, in the absence of the initiating environ- mental event. Waddington referred to this phenomenon as genetic assimila- tion, which he defined as “the conversion of an acquired character into an inherited one; or better, as a shift (towards a greater importance of heredity) in the degree to which the character is acquired or inherited” (p. 61).

Having no cross veins in their wings has no apparent adaptive value for a fruit fly but reflected merely a convenient trait Waddington could manipulate. However, in a later study, Waddington demonstrated genetic assimilation for a characteristic that could, conceivably, have an adaptive function. Flies were fed food with added salt. This produced a

high

mortality rate, and surviving flies were bred with one another. Flies exposed to high- salt diets responded

by

developing larger anal papillae, which facilitate the excretion of salt from the body. After

21

generations, eggs were placed on media containing various degrees of salt concentration. Compared with control flies, flies whose parents (and

19

generations of grandparents) had been fed high concentrations of salt developed larger anal papillae, even when grown on the low-salt concentration media. Again, a characteristic that had been acquired in response to an environmental stressor had come to be expressed in the absence of the initial event, this one being adaptive for survival.

Other researchers, both before and after Waddington, have demon- strated the phenomenon of genetic assimilation on a wide range of organisms (see Jablonka & Lamb,

1995;

Waddington, 1975). In fact, an early demon- stration of the effect was reported for the pond snail Limnaeu stagulis

by

Jean Piaget

(1896-1980;

1976). Piaget observed that the form of the snail’s shell varied with the wave action it experienced during development, which varied in different parts of the lake. When bred in the laboratory, the snails’

shells retained their unique shape over many generations. Piaget (1929/

1976)

himself advocated a form of genetic assimilation, taking an explicitly epigenetic perspective of the relation between development and evolution.

As

a more recent example, researchers have noted that an asexually reproduc- ing species of water flea (Duphina cuncullata) grows a large protective helmet when raised in the presence of the larvae of a potential predator. This enhanced defense is then passed on to daughters and, to a lesser extent, granddaughters raised in safe environments (Agrawal, Laforsch, & Tol- lrian,

1999).

54 T H E ORlGZNS OF H U M A N NATURE

With

respect to evolution, genetic assimilation and the Baldwin effect’

operate according to a three-step process. First, members of a species experi- ence a modified environment, and as a result, some survive

by

developing novel responses. This is presumably accomplished by expressing genes that are not normally expressed. This individual difference among members of the population can be seen in terms of adaptability: Those that can more readily adapt to environmental change are more likely to survive. Second, offspring of the survivors selectively breed among themselves, continuing to show adaptive responses to the now stable environment. Third, the response becomes genetically assimilated in that it is now expressed even in the absence of the environmental events that originally precipitated the change.

Mechanisms of Change

Waddington was never clear on the specific mechanism behind genetic assimilation. He was adamant that all aspects of an organism were the joint product of action of the phenotype and the environment, but obviously genetic assimilation must eventually produce some “genetic” change if a characteristic is to be expressed in the absence of the environmental event that initially evoked it. One alternative is the geneticists’ favorite, mutation, similar to that proposed

by

Baldwin for organic selection. A second possibility is that the novel environment promotes the activity of only a select set of alleles for active genes that all members of the species possess. After many generations ofselective breeding, only those alleles associated with an extreme value of a trait remain in the genotype. Thus, changes occur not in the produc- tion of new genes (via mutations), but in terms of the frequencies of different alleles for a particular trait, precisely as any trait can change in frequency in a population following conventional Mendelian analyses.

(Of

course, any single gene can have multiple effects-pleiotropy-and many different genes are likely associated with a single characteristic, making this scenario more complicated than it appears on the surface.) Third, the environmental event could have activated heretofore-dormant genes or, relatedly, served to deacti- vate certain genes, the end result being similar (a different combination of genes are involved in a particular response, relative to individuals in the pre- stressed environment). Fourth, mutations can occur in cells in the immune system, which in turn influence the germ cells, resulting in acquired immunity.

Contemporary research in genetics suggests that each of these alternatives is

’

Waddington (1975, pp. 88-91) dissociated his theory from Baldwin’s, believing that Baldwin, unlike himself, provided no role for natural selection. Although it can be difficult to interpret the precise meaning of Baldwin ( 1902), particularly considering his use of pre-Mendelian language, we see great similarities between genetic assimilation and the Baldwin effect and, for our purposes here, make no meaningful distinction between them.