Evolution And Development

Ontogeny and phylogeny_

Biologists have long sought a link between ontogeny (development) and phylogeny (evolutionary history). In 1866, Ernst Haeckel, a German evolutionist, announced his Biogenetic Law, that "ontogeny recapitulates phylogeny". His idea was that the sequence of embryonic stages mimicked the past evolutionary history of an animal. So, in humans, he argued, the earliest embryonic stages were rather fish-like, with gill pouches in the neck region. Next, he argued was an "amphibian" stage and a "reptile" stage, when the human embryo retained a tail and had a small head, and finally came the "mammal" stage, with growth of a large brain and a pelt of fine hair.

Haeckel's view was attractive at the time, but too simple. Haeckel had drawn on earlier work, including Von Baer's Law, presented in 1828, and this law can be matched with current cladistic models. Von Baer interpreted the embryology of vertebrates as showing that "general characters appear first in ontogeny, special characters later". Early embryos are virtually indistinguishable: they all have a backbone, a head and a tail (vertebrate characters). A little later, fins appear in the fish embryo, legs in the tetrapods. More specialized characters appear later: fin rays in the fish, beak and feather buds in the chick, snout and hooves in the calf, and large brain and tail loss in the human embryo.

"General characters appearing before special characters" has taken on a new meaning with the establishment of a cladistic view of phylogeny (see p. 129). Von Baer's Law draws a parallel between the sequence of development, and the structure of a clado-gram. In human development, the embryo passes through the major nodes of the clado-gram of vertebrates. The synapomorphies (see p. 130) of vertebrates appear first, then those of tetrapods, then those of amniotes, then those of mammals, of primates, and of the species Homo sapiens last.

Three other aspects of development throw light on phylogeny. Certain developmental abnormalities called atavisms, or throw-backs, show former stages of evolution, such as human babies with small tails or excessive hair, or horses with extra side toes (Fig. 6.6a), showing how earlier horses had five, four or three toes, compared to the modern one.

Vestigial structures tell similar phylogenetic stories. These are structures retained in living organisms that have no clear function, and may simply be there because they represent something that was once used. So, modern whales have, deep within their bodies, small bones in the hip region that are remnants of their hindlegs (Fig. 6.6b). Whales last had functioning hindlegs over 50 Ma in the Eocene, and the vestigial remnants are still there, even though they serve no further purpose in locomotion, and only support some muscles associated with the penis.

The third aspect of development that forms links with phylogeny is the observation that ontogenetic patterns themselves have evolved. In particular the timing and rate of developmental events has varied between ancestors and descendants, often with profound effects. This phenomenon is termed heterochrony.

Heterochrony: are human adults juvenile apes?

Heterochrony means "different time", and includes all aspects of changes of timing and rates of development. There are two forms of heterochronic change, pedomorphosis ("juvenile formation"), or sexual maturity in a juvenile body, and peramorphosis ("overdevelopment"), where sexual maturity occurs relatively late. These changes can each occur in three ways, by variation in timing of the beginning of body growth, the timing of sexual maturation or the rate of morphological development (Table 6.1).

Vf - femur pelvis

Vf - femur pelvis

Figure 6.6 Hints of ancestry in modern animals. (a) Extra toes in a horse, an example of an atavistic abnormality in development, or a throw-back, to earlier horses which had more than one toe; normal horse leg (left), extra toes (right). (b) The vestigial hip girdle and hindlimb of a whale; the rudimentary limb is the rudiment of a hindlimb that functioned 50 Ma.

Figure 6.6 Hints of ancestry in modern animals. (a) Extra toes in a horse, an example of an atavistic abnormality in development, or a throw-back, to earlier horses which had more than one toe; normal horse leg (left), extra toes (right). (b) The vestigial hip girdle and hindlimb of a whale; the rudimentary limb is the rudiment of a hindlimb that functioned 50 Ma.

Table 6.1 The processes of heterochrony: differences in the relative timing and rates of development.

Onset of growth Sexual maturation Rate of morphological development

Pedomorphosis

Progenesis - Early -

Neoteny - - Reduced

Postdisplacement Delayed - -Peramorphosis

Hypermorphosis - Delayed -

Acceleration - - Increased

Predisplacement Early - -

Figure 6.7 Heterochronic evolution in the Cenozoic brachiopods Tegulorhynchia and Notosaria. Adults of more recent species are like juveniles of the ancestor. Hence, pedomorphosis ("juvenile formation") is expressed in this example. (Based on McNamara 1976.)

Figure 6.7 Heterochronic evolution in the Cenozoic brachiopods Tegulorhynchia and Notosaria. Adults of more recent species are like juveniles of the ancestor. Hence, pedomorphosis ("juvenile formation") is expressed in this example. (Based on McNamara 1976.)

In studying heterochrony, it is necessary to have a robust phylogeny of the organisms in question, an adequate fossil record of the group, and a sound set of ontogenetic sequences for each species. This allows the paleontologist to compare juveniles and adults throughout the phylogeny. A classic example is human evolution. It seems obvious that human adults look like juvenile apes, with their flat faces, large brains and lack of body hair. These would imply a pedomorphic change in humans with respect to the human/ ape ancestor. However, other characters do not fit this pattern. For example, developmental time in humans is far longer than in apes and ancestral forms, a feature of peramorpho-

sis, and hyperomorphosis in particular (developmental time is longer, but rate of morphological development is not faster). Thus, heterochronic changes can occur in different directions in different characters, a phenomenon called mosaic evolution.

In a classic study, McNamara (1976) suggested that species of the Cenozoic brachio-pod Tegulorhynchia evolved into Notosaria by a process of heterochrony (Fig. 6.7). The main changes were a narrowing of the shell, a reduction in the number of ribs in the shell ornament, a smoothing of the lower margin, and an enlargement of the pedicle foramen (the opening through which a fleshy stalk attaches the animal to a rock). These changes

Figure 6.8 Heterochronic evolution in the Triassic rhynchosaurs. The skull of adult (A) Late Triassic forms developed beyond the size and shape limits seen in earlier Triassic adult forms. Here, the juveniles (J) of the descendants resemble the ancestral adults, and this is thus an example of peramorphosis ("beyond formation"). (Based on Benton & Kirkpatrick 1989.)

Figure 6.8 Heterochronic evolution in the Triassic rhynchosaurs. The skull of adult (A) Late Triassic forms developed beyond the size and shape limits seen in earlier Triassic adult forms. Here, the juveniles (J) of the descendants resemble the ancestral adults, and this is thus an example of peramorphosis ("beyond formation"). (Based on Benton & Kirkpatrick 1989.)

related to a shift of habitats from deep to shallow high-energy waters: the large pedicle allowed the brachiopod to hold tight in rougher conditions, and the other changes helped stabilize the shell. The developmental sequence of the ancestral species T. boongeroo-daensis shows that its descendants are like the juvenile stage. Hence, pedomorphosis has taken place along a pedomorphocline ("child formation slope"). It is harder here to determine which type of pedomorphosis has taken place; perhaps it was neoteny.

A second example illustrates a peramor-phic trend. Rhynchosaurs were a group of Triassic herbivorous reptiles. Later species had exceptionally broad skulls as adults, which gave them vast muscle power to chop tough vegetation. Juvenile examples of these Late Triassic rhynchosaurs retain the rather narrower skulls of the ancestral adult forms (Fig. 6.8). Hence, the evolution of the broad skull is an example of peramorphosis, along a peramorphocline ("overdevelopment slope"). The adult Late Triassic rhynchosaurs are larger than earlier forms, which implies that sexual maturation was delayed while the body continued to grow (hypermorphosis) or the rate of morphological development increased in the same duration of ontogeny (acceleration).

Developmental genes_

It has been understood since the time of Darwin that the external form, or phenotype, of an organism is controlled by the genotype, the genetic code (see p. 121), but the exact mechanisms have been unclear. At one time people thought there was roughly one gene for each morphological attribute. Some characters seem to be inherited in a unitary manner - you inherit blond, black or red hair from one or the other or both of your parents, and so it might be reasonable to assume that there is a gene variant for each color. But most phenotypic characters are inherited in a much more complex manner, and it is clear that there is no single gene that controls the shape of your nose, the length of your legs or your mathematical ability.

Some clarity has now been shed on how genes control form. There are a number of developmental genes that are widely shared among organisms and that determine fundamental aspects of form such as symmetry, anteroposterior orientation and limb differentiation. Since the 1980s a major new research field has emerged, sometimes called "evo-devo" (short for evolution-development), that investigates these developmental genes. This field is exciting for paleontologists because the developmental genes control aspects of form on a macroevolutionary scale, and so major evolutionary transitions can be interpreted successfully in terms of developmental genes.

The most famous developmental genes are the homeobox genes, identified first in the experimental geneticist's greatest ally, the fruit fly Drosophila, but since found in a wide range of eukaryotes from slime molds to humans, and yeast to daffodils. Homeobox genes contain a conserved region that is 180 base pairs long (see p. 186) and encodes transcription factors, proteins that switch on cascades of other genes, for example all the genes required to make an arm or a leg. In this sense homeobox genes are regulatory genes; they act early in development and regulate many other genes that have more specialist functions.

The Hox genes are a specific set of homeo-box genes that are found in a special gene cluster, the Hox cluster or complex that is physically located in one region within a chromosome. Hox genes function in patterning the body axis by fixing the anteroposterior orientation of the early embryo (which is front and which is back?), they specify positions along the anteroposterior axis, marking where other regulatory genes determine the segmentation of the body, especially seen in arthropods (see p. 362), and they also mark the position and sequence of differentiation of the limbs (Box 6.3).

Box 6.3 Hox genes and the vertebrate limb

One of the greatest transitions of form in vertebrate evolution was the remodeling of a fish into a tetrapod, a process that occurred more than 400 Ma in the Devonian (see p. 442). The fossils show how the internal skeleton of a swimming fin was transformed into a walking limb. A crucial part of this repatterning from fin to limb seemed to be the pentadactyl limb, the classic arm or leg with five fingers or toes seen in humans and most other tetrapods. But then paleontologists began to find Late Devonian tetrapods with six, seven or eight digits. How could this be explained in a world where there was supposed to be a gene for each digit, and five was the norm?

The tetrapod limb can be divided into three portions that appear in the embryo one after the other, and that appeared in evolutionary history in the same sequence. First is the proximal portion of the limb, the stylopod (the upper arm or thigh), then the middle portion of the limb, the zeugopod (the forearm or calf), and finally the distal portion, the autopod (the hand and wrist or foot and ankle).

This evolutionary sequence is replicated during development of the embryo (Shubin et al. 1997; Coates et al. 2002; Tickle 2006; Zakany & Duboule 2007). At an early phase, the limb is represented simply by a limb bud, a small lateral outgrowth from the body wall. Limb growth is controlled by Hox genes. Early in fish evolution, five of the 13 Hox genes, numbered 9-13, were coopted to control limb bud development. Manipulation of embryos during three phases of development has shown how this works (Fig. 6.9a). In phase I, the stylopod in the limb bud sprouts, and this is associated with expression of the genes HoxD-9 and HoxD-10. In phase II, the zeugopod sprouts at the end of the limb bud, and the tissues are mapped into five zones from back to front by different nested clusters of all the limb bud genes HoxD-9 to HoxD-13. Finally, in phase III, the distal tip of the lengthening limb bud is divided into three anteroposterior zones, each associated with a different combination of genes HoxD-10 to HoxD-13. Phases I and II have been observed in bony fish development, but phase III appears to be unique to tetrapods.

In the development of vertebrate embryos, there is no fixed plan for every detail of the limb. A developmental axis runs from the side of the body through the limb, and cartilages condense from s

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  • Alvin
    What is an example of Heterochrony?
    8 years ago

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