Development and Evolutionary Change

Transcription

1 21 Development and Evolutionary Change Among many fish species, the sex of other members of the group in which an individual fish lives its social environment determines its sex. For example, anemonefish (also known as clownfish) always begin life as males. Anemonefish live in social groups of five or so individuals living within a single sea anemone. The group s leader is the largest fish in the group and is also its only female. If the female is removed from the group, the largest male in the group changes sex and becomes a female. Cleaner wrasse, on the other hand, first mature sexually as females. The largest female in a group eventually changes sex to become a male. A female wrasse can be induced to change sex earlier if the dominant male of the group is removed. Within a few hours, the former female adopts male behavior, and within 10 days this new male is producing functional sperm. The genome has often been believed to provide a blueprint for an organism s development. But fish that change sex in response to their social environment demonstrate that an organism s development is not determined entirely by its genes. Genes not only give orders; they also take orders. Thus, an organism s genome is more like a recipe. The final product the phenotype may depend on how the ingredients are mixed and the conditions during preparation and cooking. Genes are molecules that encode other molecules, which in turn affect different parts of an organism. There are no genes for complex structures such as eyes, or for behavior patterns. The genome encodes instructions for making enzymes, receptors, signal molecules, structural molecules, and so forth. The phenotype of an adult organism comes into being as a result of interactions between genes, their products, and the environment. In this chapter we will look at the mechanisms of development from an evolutionary perspective. We will show how mutations in the genes that regulate development can enable new structures to evolve. We will see how the modular nature of organisms can allow structural changes in the phenotype even when the gene sequences themselves have not changed. We will also describe how interactions between the environment and developmental processes help adapt organisms to their environments. When Size Determines Sex All anemonefish begin life as males. The largest male in the social group will change sex to become the group s only female.

2 430 CHAPTER TWENTY-ONE Evolution and Development Charles Darwin viewed evolution as descent with modification. He explained similarities among organisms as a result of their descent from a common ancestor, and he explained differences among them as a result of natural selection, which adapts them to different environments. Darwin s theory of descent with modification led to the recognition that the results of evolution could be visualized as a tree of life. The tree s root is the ancient common ancestor of all life; its branches represent the divergence of lineages of evolving organisms over time. Darwin recognized that morphological patterns could be modified by changes in the processes that regulated the growth of an organism from egg to adulthood, but did not explore this theme in great detail. However, in The Origin of Species, he showed how similarities among embryos could be used to infer relationships among groups of organisms. For example, he concluded that barnacles are crustaceans (a large group that also includes shrimp and crabs) on the basis of similarities between larval forms, even though adult barnacles look very different from other crustaceans (Figure 21.1) Early in the twentieth century, embryology and genetics were regarded as a single science. But in the 1920s, geneticists turned their attention almost exclusively to the transmission of inherited characteristics from adult organisms to their offspring. Embryologists turned their attention to the expression of those characteristics during development. That is, geneticists were interested in how genes determine the number of bristles on a fruit fly s back, while embryologists were interested in how the fly forms its back. The two sciences progressed without much intellectual contact until late in the twentieth century, when they began to come together to form the new discipline of evolutionary developmental biology. Evolutionary developmental biologists investigate how the course of evolution has been influenced by heritable changes in the development of organisms. Like geneticists, they are interested in the inheritance of the characteristics of organisms. Developmental biologists now study how changes in the genes that regulate development affect the adult forms of organisms. They also study how those genes have changed during the course of evolution. To understand large evolutionary changes, such as the evolution of eyes, wings, and flowers, biologists study both developing and adult organisms, because the agents of evolution work not only on adults but on the recipes for making adults. Evolutionary developmental biologists look for alterations both in the genes that regulate development and in the genes for their target proteins. Early discoveries showed that many of the genes regulating development are highly conserved that is, the sequences of these genes have changed remarkably little throughout the course of evolution of multicellular organisms. Let s look at these similarities and find out why the genes that govern development have changed so little over evolutionary time. Gooseneck barnacles (Lepas sp.) Brine shrimp (Artemia salina) 21.1 Similarities In Early Developmental Stages Can Be Used to Infer Relationships Adult barnacles do not clearly resemble adults of other crustaceans, such as brine shrimp (right), but Charles Darwin observed the similarities between their larvae (lower photos) and concluded correctly that these animals share a recent common ancestor. Larvae Adults

3 DEVELOPMENT AND EVOLUTIONARY CHANGE The Mouse Pax6 Gene Causes Eye Development in Drosophila The Pax6 gene for eye development is ancestral to both arthropods and vertebrates. This micrograph shows a compound eye emerging in the leg of a fruit fly in which mouse Pax6 cdna was expressed. Development uses the same sets of genes throughout the animal kingdom Many of the genes that regulate development in very different animal species are remarkably similar. The compound eyes of fruit flies (Drosophila) and the camera-like eyes of house mice (Mus musculus) differ greatly in their structure and functioning, but many of the same genes instructs cells to form eyes in both animals. The genetic instructions for eye development in the two species are so similar that fruit fly cells that would normally form part of a leg will form an eye (a Drosophila eye) when a mouse Pax6 gene is expressed in them (Figure 21.2). Most motile animals (animals that move through their environment as a result of their own exertions) have bilaterally symmetrical bodies with a head (anterior) and a tail (posterior) end, and the bodies of many of them are divided into segments (see Chapter 32). The same sets of homeobox genes provide positional information to cells along the anterior-posterior axis of the body in both insect and human embryos. For example, both the Drosophila gap genes ems, tll, and otd and the homologous genes of vertebrates are expressed in the anterior regions of the brain (Figure 21.3). When certain insect homeotic genes are mutated, the segments differentiate in the wrong way. The bithorax mutation causes the developing insect to form two sets of forewings rather than the normal one pair (Figure 21.4a), and the Antennapedia mutation results in the formation of legs where the antennae should be (see Figure 19.16). In vertebrates, altering the expression patterns of some Hox genes can change lumbar (abdominal) vertebrae into thoracic (ribbed) vertebrae (Figure 21.4b). Altering the expression of other genes can replace neck bones with duplications of the ear bones and jaw. Thus the instructions for forming embryos are provided by homologous genes in vertebrates and invertebrates, even though the structures formed from those instructions are very different. The enormous variation of morphological forms found in the animal kingdom is underlain by a common set of instructions. These instructions have been con- Thorax Abdomen Anterior Anterior brain Posterior brain Posterior Drosophila Forebrain Hindbrain Spinal cord Homologous genes are shown in the same color. Vertebrates 21.3 Genes Show Similar Expression Patterns Homologous genes for certain transcription factors are expressed in similar patterns along the anterior posterior axes of both insects and vertebrates.

4 432 CHAPTER TWENTY-ONE Second thoracic segment Normal wing 21.4 Altering Homeobox Genes Changes Morphology (a) Deletion of the Ubx gene in Drosophila converts the third thoracic segment, which does not normally bear wings, into a duplication of the second thoracic (forewing-bearing) segment. (b) Deletion of the Hoxc-8 gene in mice transforms a lumbar (abdominal) vertebra into a copy of a thoracic (ribbed) vertebra. (a) Third thoracic segment Duplicate wing (b) Extra rib served in thousands of species that display an incredibly vast array of seemingly unrelated morphologies. However, the vast differences in morphological form that result from such similar genetic instructions means that the instructions cannot be the whole story. The anterior-posterior axes of both human and fruit fly embryos are specified by the same genes, but humans don t develop wings. Humans use Pax6 to specify eye-forming regions, but the human visual system forms from different precursor structures than the fly system does. So there must be important differences as well as important similarities. Both similarities and differences are expected under descent with modification, but how can differences in developmental genetics explain structural differences? Regulatory Genes and Modularity: Modifying Morphology How can the development pattern of an embryo change without resulting in an adult organism that cannot function well? Such changes are possible because embryos, like adults, are made up of modules. A module is a self-contained unit that is part of a larger unit. The form of each module may be changed independently of the other modules in the overall unit. Thus the form of a developing animal s heart can change independently of changes in its limbs because the genes that govern heart formation do not affect limb formation, and vice versa. Two major ways in which changes in the genes that regulate development can lead to evolutionarily important morphological changes have been elucidated during the past several decades: Mutations in genes that regulate developmental processes Changes in the time or place of expression of developmental regulatory genes Both of these pathways of evolution are made easier by the modular nature of most organisms. Mutations can result in new phenotypes Insects are highly modular organisms; in Chapter 19 we saw the precision of the segmentation process in insect development. Insects provide examples of the evolution of morphological changes through mutations in the genes encoding transcription factors that regulate segmentation. For example, all arthropods (see Chapter 33) possess the homeotic gene Ultrabithorax (Ubx), but the insect Ubx gene has a mutation not found in the other arthropods (Figure 21.5). The Ubx protein transcribed from this mutated gene represses expression of the distal-less gene (dll), which is essential for leg formation. The Ubx protein of insects is expressed in the abdomen where it represses dll. As a result, insects have only six legs, none of which grow from the abdominal segments. In contrast, the Ubx protein of other arthropods such as millipedes, centipedes, spiders, mites, and crustaceans do not repress the expression of dll. Consequently, those animals all have abdominal appendages. The evolution of the webbed feet of ducks is an example of an evolutionary change resulting from an altered spatial expression pattern of a regulatory gene. Ducks have webs that connect their toes, but chickens and most other birds do not. The developing feet of early embryos of both ducks and chickens have webs (as do those of humans; see Figure 19.11). A particular gene is expressed in the spaces between the developing bones of the toes. This gene encodes a protein called bone morphogenetic protein 4 (BMP4). This protein instructs the cells between the developing toes to undergo apoptosis programmed cell death. The death of these cells destroys the webbing between the toes. Embryonic duck and chicken hindlimbs both express BMP4 in the webbing between the toes, but they differ in the expression of a BMP inhibitor protein, called Gremlin (Figure 21.6). Gremlin expression occurs around the digits in both chick and duck hindlimbs. In ducks, but not in chickens, the gremlin gene is also expressed in the webbing cells. The Gremlin protein prevents the BMP4 protein from signaling for cell death in the webbing; the result is a

5 Figure 21.5 A Mutation Changed the Number of Legs in Insects In the insect lineage (blue) of the arthropods, a mutation in the Ubx gene resulted in a protein that inhibits a gene that is required for legs to form.because insects express Ubx in their abdominal segments, no legs grow from these segments. Other arthropods, such as centipedes, do grow legs from their abdominal segments. Common ancestor Change in protein structure Fly Mosquito Butterfly Moth Beetle Springtail Shrimp Spider Centipede Onycophoran Beetle Centipede In the insect lineage, a mutation in the Ubx homeotic gene prevents legs from forming in the abdominal segments. webbed foot. Experimental application of the Gremlin protein to chick hindlimbs converts them into ducklike feet (Figure 21.7). The timing of a gene s expression can affect morphology Modularity also allows the relative timing of two different developmental processes to shift independently of one another, a process called heterochrony. That is, the genes regulating Most arthropods have legs growing from their abdominal segments. the development of one module (say, the eyes of vertebrates) may be expressed at different times in different species, relative to genes regulating development of other modules. Heterochrony has been widely studied in salamanders, where extensive examples of this phenomenon are seen. The case of two salamander species of the genus Bolitoglossa illustrates how heterochrony can result in new morphology. Purple dye marks the presence of BMP4. Chick limbs do not express Gremlin (a BMP inhibitor). Red dye shows the pattern of cell death (apoptosis). Chick hindlimb In the chicken, webbing undergoes apoptosis, resulting in the separated toes of the adult. Duck hindlimb Webbing in the adult duck s foot remains intact. Duck limbs express Gremlin (arrows) Changes in gremlin Expression Correlate with Changes in Hindlimb Structure The upper row of photos shows the development of the foot of a chicken; the lower row shows the development of the foot of a duck. Expression of Gremlin protein in the duck foot blocks BMP4 and prevents the embryonic webbing from undergoing apoptosis.

6 434 CHAPTER TWENTY-ONE EXPERIMENT Question: Will adding Gremlin protein (an inhibitor of BMP4) to a developing chick foot transform the chick foot into a ducklike form? METHOD Open up chicken eggs and carefully add Gremlin-secreting beads to the interdigital (web) regions of one embryonic chick hindlimb. Add beads that do not contain Gremlin to the other hindlimbs (controls). Close the eggs and observe limb development. (a) B. rostratus (terrestrial) The digits of the adult terrestrial salamander extend past the webbing. (b) B. occidentales (arboreal) The webbed feet of this arboreal species resemble those of the juvenile B. rostratus. RESULTS Gremlin added In the hindlimbs in which Gremlin was secreted, the webbing does not undergo apoptosis, and the hindlimb resembles that of a duck. The control hindlimbs develop the normal chicken form. Control 21.8 Heterochrony Created an Arboreal Salamander (a) The foot of an adult Bolitoglossa rostratus,a terrestrial salamander. (b) The foot of B. occidentalis,a closely related arboreal salamander. Conclusion: Changes in gremlin gene expression could cause the changes in morphology, allowing duck hindlimbs to retain their webbing and chick limbs to lose it Changing the Form of an Appendage In this experiment, chick hindlimbs exposed to Gremlin-secreting beads developed ducklike webbed feet. The webbing between the feet of the larvae of most species of salamanders disappears as the animals mature, resulting in toed feet suited to getting around on the ground (Figure 21.8a). But if expression of the genes that dissolve the webbing slows, the digits do not expand as the rest of the body matures. These juvenile webbed feet (Figure 21.8b) can act like suction cups, allowing the animal to adhere to tree branches. This ability opens up a new, arboreal way of life to the new species that possesses it. Modularity also allows structural changes to evolve via gene duplication. When a gene is duplicated, one of the copies can evolve a new function without disrupting the organism, as long as the other copy is still performing the original function. We will discuss this process in detail in Chapter 26. Plant Development and Evolution Rapid progress has been made during the past decade in identifying the genes that regulate growth and cell differentiation in plants. Much of this information has come from the sequencing of the complete genome of Arabidopsis thaliana. About 1,500 of its nearly 26,000 genes encode transcription factors that turn on or repress the expression of genes by binding to specific DNA sequences. More than half of the known families of transcription factor genes are found in all eukaryotes, but many others are found only in plants. The ones that are restricted to plants have evolved independently in plants since plants and animals diverged from protist ancestors hundreds of millions of years ago. Although plants and animals share many regulatory genes, plants differ from animals in several important ways that affect their development: Plant cells do not move relative to one another. As we noted in Chapter 19, plant cells do not move around within the plant body during development. Changes in the shape of a developing plant result from cell proliferation and elongation. In contrast, as we saw in Chapter 20, complex movements of cells characterize the development of animal embryos. These movements determine how the shapes of adult animals develop. Future reproductive cells are not set aside early during plant development. Instead, throughout their lives, plants continue to produce clusters of undifferentiated, actively dividing cells, called meristems. Meristems allow a plant to develop and form new organs, such as stems, roots, leaves, and flowers, as long as it grows. In contrast, during animal development, organs are formed according to highly regulated developmental schedules that take

7 DEVELOPMENT AND EVOLUTIONARY CHANGE 435 place only once during an individual s lifetime. We humans make an arm only once in our life cycle, during our embryonic development. Plants have tremendous developmental plasticity. If an herbivore eats part of a plant, leaf meristems may grow out and replace the lost part. The new leaves may also produce chemicals that defend them against herbivores. And, as we will see later in this chapter, plant growth responds dramatically to temperature and light. This ability of an organism to change its development in response to environmental conditions is called developmental plasticity. Despite these important differences, members of two families of genes that encode transcription factors the MADS box genes and the homeobox genes regulate important developmental processes in both plants and animals (see Chapter 19). However, in plants, these genes govern the development of unique structures roots, stems, leaves, and flowers found only in that kingdom. Much more is known about the genetic control of development in Arabidopsis than in any other plant, but enough is known about other plants to suggest that many genes regulating plant development are shared by many species of plants. For example, genes that result in early flowering in Arabidopsis have a similar effect in aspen trees. Why do plants and animals still share so many of the genes that regulate their development, even though they have been evolving separately for such a long time and produce such different tissues and organs? Part of the reason, as we saw above, is that the modular construction of multicellular organisms allows different parts of their bodies to change independently of one another. Another part of the answer involves how the genomes of organisms change, a topic that we will discuss in detail in Chapter 26. Plants have greater developmental plasticity than animals because developmental plasticity is especially valuable for a sessile organism. Plants cannot move to another place if environmental conditions deteriorate where they are growing, nor can they move to escape from their predators and parasites. Unlike most animals, however, they can be partly eaten but still survive. The combination of repeated production of meristems and developmental plasticity compensates for a plant s lack of mobility. Environmental Influences on Developmental Patterns Organisms are adapted to their environments in part because their development has been molded by the agents of evolution. However, the idea that the environment plays an important role in the development of organisms was downplayed until very recently. Part of the reason for this neglect is that, for convenience, developmental biologists studied small organisms that develop rapidly and whose development does not change dramatically in the laboratory under controlled conditions. As we saw in Chapter 1, control of conditions is an important component of the scientific method. But these studies fostered the misleading view that genes had an autonomous existence apart from environmental signals. Now we know that the development of many organisms is exquisitely sensitive to environmental conditions. Numerous species possess a great deal of developmental plasticity the ability to express different phenotypes under different environmental conditions. In other words, a single genotype may encode a range of phenotypes, and signals from the environment may determine what phenotype is expressed. But how should organisms respond to signals from the environment in order to develop adaptively? No single way of responding to signals from the environment results in adaptation because what environmental signals tell an organism varies with the type of signal. We can divide signals from the environment into two major types, based on their significance and how organisms should respond to them: Environmental signals that are accurate predictors of future conditions. Some of these signals always occur, but organisms may develop without ever encountering others. In either case, we would expect the developmental processes of organisms to respond adaptively to these signals. Environmental signals that are poorly correlated with future conditions. We would expect organisms to fail to respond to such signals. Let s look at some of the developmental responses of organisms to these different types of signals. Organisms respond to signals that accurately predict the future Seasonal changes in day length occur every year, and these changes are accurate predictors of some future environmental conditions. Increasing day lengths accurately predict the approach of spring and summer; decreasing day lengths accurately predict the coming of fall and winter. Temperature changes also accompany the seasons and signal future environmental conditions. In most tropical regions, wet and dry seasons alternate in a regular pattern during the year. Developing organisms respond to such signals in such a way that the adults they become are adapted to the predicted conditions. The West African butterfly Bicyclus anynana has two color forms. The dry-season form matches the dead brown leaves on the dry-season forest floor, where the butterfly rests much of the time. The more active wet-season form has a white line along the wing and conspicuous ventral hindwing eyespots.

8 436 CHAPTER TWENTY-ONE Dry-season form Larva <20 C Decreased distal-less expression Distal-less protein Wet-season form >24 C 21.9 Development of Eyespots in Bicyclus anynana Responds to Temperature Warm temperatures during pupation increase the expression of the distal-less gene, resulting in eyespot formation. At cooler temperatures, distal-less expression is decreased, and the eyespots fail to form. Increased distal-less expression These eyespots deceive predatory lizards and birds into attacking the wing, rather than the butterfly s actual eye, increasing the butterfly s chances of escape. Temperature during pupation determines the color form of the adult butterfly. Pupae developing in the soil experience cooler temperatures during the cooler nights of the dry season. Pupae developing under temperatures less than 20 C produce the dry-season form; temperatures above 24 C produce the wet-season color form. In the late larval stages, transcription of the distal-less gene is restricted to several small areas that have the potential to become the centers of eyespots. During pupal development, the area over which distal-less is expressed increases with temperature, resulting in eyespots on adults that develop from pupae exposed to warm temperatures (Figure 21.9). Thus, by responding to an environmental signal temperature the (a) Catkins butterflies develop a form that adapts them to the conditions they will encounter as adults. Another example of developmental plasticity in response to seasonal changes occurs in the moth Nemoria arizonaria, in this case at the larval stage. This moth produces two generations each year. Eggs hatch in spring, and the larvae that hatch from them (caterpillars) feed on oak flowers (catkins). These larvae complete their development, form pupae, and transform themselves into adult moths in summer. These moths then lay their eggs on oak trees. The larvae that hatch from these eggs eat oak leaves, complete their development, and lay their eggs on oak branches. These summer eggs overwinter and hatch the following spring. The spring caterpillars resemble the catkins on which they feed (Figure 21.10a); the summer caterpillars that feed on oak leaves resemble small, year-old oak branches (Figure 21.10b). Thus, both types of caterpillars are well camouflaged in the environment in which they feed. An experimenter was able to convert spring caterpillars into summer caterpillars by feeding them oak leaves. Apparently some chemical in the oak leaves induces them to develop the twiglike summer form. To complete their development, some organisms need help from another species. Such a requirement could not evolve unless individuals of the other species were reliably present. House mice that are raised in microbe-free environments do not have the bacteria that normally colonize their guts. These mice also do not have normal capillary networks in their intestines. The gut bacteria induce gene expression in the mouse intestine, without which normal capillary development does not occur. In nature, all mice get the bacteria. Caterpillars The Spring and Summer Forms of a Caterpillar Differ (a) Spring caterpillars of Nemoria arizonaria resemble oak catkins. (b) Summer caterpillars of the same species resemble oak twigs. (b)

9 DEVELOPMENT AND EVOLUTIONARY CHANGE 437 Some conditions that accurately predict the future may not always occur We have discussed responses to environmental signals that always occur. However, many other changes in an organism s environment are uncertain. Predators may or may not be active in an organism s environment. An individual may live under crowded or uncrowded conditions. The sexes and ages of its associates may change. Nevertheless, if such changes have occurred frequently during the evolution of a species, evolved developmental plasticity may allow individuals to respond to them. For example, as we saw at the beginning of this chapter, individuals of some fish species change sex in response to alterations in their social environment. The social environment, including the sexes of others in the social group, determines which is the most adaptive sex for an individual to have at a particular time. Similarly, individuals that could sense the presence of predators in their environment and change their development so as to become less likely to be eaten by them would be more likely to survive than individuals whose development did not respond to the presence of predators. Thus, developmental responses to predators have evolved in numerous species. For example, when water fleas (Daphnia cucullata) encounter predatory larvae of the fly Chaeoborus, the helmets on the top of their heads grow to twice their normal size (Figure 21.11). The fly larvae can ingest Daphnia with large helmets only with difficulty. Helmet induction also occurs if Daphnia are exposed to water in which the fly larvae have been swimming. Moreover, the offspring that are developing in the abdomens of mothers with induced large helmets are born with large helmets. There is a trade-off, however: Daphnia with large helmets produce fewer eggs than do Daphnia with small helmets. Otherwise, we would expect all individuals to develop large helmets. Tadpoles of the spadefoot toad (Scaphiopus couchii), which breeds in ephemeral ponds in the arid southwestern United States, respond developmentally if their pond begins to dry up while they are growing. At the time she lays her eggs, a mother toad cannot know how long the pond will persist, because that depends on unpredictable future rainfall. If the pond dries up completely before the tadpoles development has been completed, they will die. Some spadefoot tadpoles respond to crowding in a shrinking pond by developing a wider mouth and powerful jaw muscles. They complete their development rapidly before the pond dries up by eating other tadpoles. Light exerts a powerful influence on plant development. Low light conditions stimulate the elongation of cells, so that plants growing in the shade become spindly (Figure 21.12). It is obvious why this response is adaptive: A spindly plant is more likely to reach a patch of brighter light than a plant that remains compact. And because they have meristems, plants can continue to respond to light as long as they grow Predator-Induced Developmental Plasticity in Daphnia This scanning electron micrograph shows the predator-induced form of Daphnia (left), with an enlarged helmet, and the normal form of the crustacean (right). These two individuals are genetically identical from a single asexually produced clone Light Seekers The bean plants on the left were grown experimentally under low-light conditions. The plant s cells have elongated in response to low light, and the overall plant has become spindly. The control plant on the right was grown in normal light conditions.

10 438 CHAPTER TWENTY-ONE Organisms do not respond to environmental signals that are poorly correlated with future conditions We would expect organisms to evolve to ignore environmental signals that are poorly correlated with future conditions, because any responses to those signals would probably be inappropriate. Consider, for example, seed production by plants. The amount of energy a growing plant has available to allocate to seed production depends, among other things, on temperature, rainfall, and the sizes and numbers of its neighbors. But the seeds the plant produces will germinate in future years, with different and unknowable rainfall patterns and densities of neighbors. Plants respond to changing environmental conditions by varying their size, shape, number of flowers, and number of seeds, but they produce seeds of a nearly constant size (Figure 21.13). A seedling that germinates from a large seed will survive better under conditions of intense competition than a seedling that germinates from a small seed because it can grow larger using the energy in the seed. But, for a given amount of energy, a mature plant cannot produce as many large seeds as small seeds. So, if the next generation of plants grows under more favorable conditions, plants that produced a larger number of smaller seeds in the previous year will (a) (b) Mean seed weight (g) Number of capsules Number of plants/m Seeds per capsule Capsules per plant Number of plants/m Seed Production (a) No matter how crowded or uncrowded the conditions under which these plants were grown, the seeds they produced were about the same size. (b) The number of seeds the plants produced dropped dramatically in more crowded conditions Number of seeds have more surviving offspring. Therefore, it is not surprising that plants do not change the sizes of the seeds they produce in response to the conditions under which they grow. Seed size is adjusted to the average conditions encountered by plants over many generations. Organisms may lack appropriate responses to new environmental signals As we have seen, organisms can respond adaptively to environmental signals that have occurred frequently during their recent evolutionary histories. But we would not expect organisms to have evolved useful responses to environmental signals that they have not encountered before. The lack of useful developmental responses to new environmental events is an important current problem because modern human societies have changed the environment in so many ways. Humans release thousands of new chemical compounds into the environment, some of which disrupt normal development. For example, more than 7,000 deformed infants were born to women who took a drug called thalidomide as a mild sedative during pregnancy. Human embryos are especially sensitive to thalidomide for the first days after conception, a time when many organs are forming. And as we saw in Chapter 1, deformed frogs are appearing at high frequencies in some environments. Pieter Johnson s experiments suggested that a parasite causes some of these deformities. Further experiments have shown that tadpoles growing in ponds contaminated by certain pesticides are less able to resist parasite infection than tadpoles growing in pesticide-free ponds. Understanding how and why such chemicals affect development may help us devise substitutes that have fewer or no adverse effects. Learning: A Modification of Development A nearly universal modification of development in response to environmental variation is learning. As you know from your struggles to absorb the content of this book, which we authors have struggled just as mightily to compose, learning is costly. Learning takes much effort and time, during which an individual cannot do other useful things. But learning can continue throughout adult life, albeit with continuing costs. Learning also allows an individual to adjust its behavior to the physical, biological, and social environment in which it matures. As we will see in Chapters 46 and 52, learning is especially important in species with complex social systems. Individuals of these species must learn the identities and individual characteristics of many associates and adjust their behavior accordingly. Meanwhile, bear in mind that as difficult as learning may be, ignorance is even more costly.

11 DEVELOPMENT AND EVOLUTIONARY CHANGE 439 Evolutionary developmental biologists are generating new insights into the evolution of the diversity of organisms. This rapidly developing field is providing us with new information with which to understand the form of the Tree of Life. In Part Four of this book we will describe the history of life on Earth, and we will show how the agents of evolution act on the survival and reproductive success of adult organisms; that is, we will discuss the approach to evolution that has been developed by population geneticists and ecologists. The insights generated by that approach complement those derived from evolutionary developmental biology that we have just discussed. Together, they constitute a more complete view of the evolution of life on Earth. Chapter Summary Evolution and Development The field of evolutionary developmental biology unites embryology, ecology, and genetics. It is generating new information that helps us understand how the recipes for making organisms interact with environmental signals to produce functional organisms. Relationships among organisms can often be inferred by similarities in their embryonic or larval features. Many of the genes regulating development have changed very little throughout animal evolution. The same sets of genes are involved in specifying the anteriorposterior axis in both vertebrates and invertebrates. Review Figure 21.3 Regulatory Genes and Modularity: Modifying Morphology Major morphological changes can result from mutations in developmental regulatory genes or from alterations in the time or place of expression of these genes. Review Figures 21.5, See Web/CD Tutorial 21.1 Modularity allows morphological changes to occur without disrupting the entire organism. Heterochrony, a shift in the relative timing of two different developmental processes, can result in new morphology. Review Figure 21.8 Plant Development and Evolution Plants differ from animals in important ways that influence how they develop. Plant cells do not move relative to one another during development. In addition, the reproductive cells are not set aside early during plant development. Instead, plants continue to produce undifferentiated meristems as long as they grow. And plants have great developmental plasticity. See Web/CD Activity 21.1 Despite these differences, plants have MADS box genes and homeobox genes, some of which are shared with animals, although they govern the development of structures unique to plants. Environmental Influences on Developmental Patterns A genotype may encode a range of phenotypes. Developmental plasticity is the ability to express different phenotypes under different environmental conditions. Some environmental signals always occur and accurately predict future conditions. Others may or may not occur, but are good predictors of future conditions when they do appear. The development of organisms often responds adaptively to such signals. Review Figure 21.9 Many organisms have the ability to detect the presence of predators and alter their development to reduce the likelihood that they will be attacked. Organisms evolve to not respond to environmental signals that are poor predictors of future conditions. Plants respond to light and other environmental conditions by changing their shapes and the number of flowers or seeds they produce, but not the sizes of their seeds. Review Figure Knowledge of how developing organisms are influenced by chemical agents that disrupt normal development may help us find alternative materials to use that are less damaging. Learning: A Modification of Development Learning is a costly way of modifying development, but it can continue throughout adult life, and it allows an individual to adjust its behavior to the environment in which it matures. Self-Quiz 1. Genes provide recipes rather than constituting blueprints because a. genetic instructions do not specify the form of the adult organism. b. an organism s development is not determined entirely by its genes. c. genes take orders as well as giving orders. d. genes encode other molecules, which in turn affect different parts of an organism. e. all of the above 2. Genetics and developmental biology evolved without much intellectual contact during much of the twentieth century because a. developmental biologists did not believe that development was genetically controlled. b. geneticists underestimated the degree to which the environment could influence development. c. geneticists and developmental biologists competed for research funds and therefore emphasized the differences between their disciplines. d. geneticists turned their attention to the heritability of traits, whereas embryologists turned their attention toward the unfolding of genetic instructions during the development of individuals. e. the genes that control development were of little interest to geneticists because they do not influence the ability of individuals to transmit their genes to offspring. 3. Homeobox genes determine the positions of cells along a. the anterior-posterior axis of the bodies of both insect and human embryos. b. the anterior-posterior axis of the bodies of insects, but not of vertebrates. c. the anterior-posterior axis of the bodies of vertebrates, but not of insects. d. the dorsal-ventral axis of the bodies of both insect and human embryos. e. the dorsal-ventral axis of the bodies of vertebrates only.

12 440 CHAPTER TWENTY-ONE 4. Ducks have webbed feet and chickens don t because a. ducks need webbed feet to swim, whereas terrestrial chickens do not. b. both duck and chicken embryos express BMP4 in the webbing between the toes, but the gremlin gene is expressed only in the webbing cells of ducks. c. both duck and chicken embryos express BMP4 in the webbing between the toes, but the gremlin gene is expressed only in the webbing cells of chickens. d. only duck embryos express BMP4 in the webbing between the toes. e. only chick embryos express BMP4 in the webbing between the toes. 5. Modularity is important for development because it a. guarantees that all units of a developing embryo will change in a coordinated way. b. coordinates the establishment of the anterior-posterior axis of the developing embryo. c. allows changes in the genes to change one part of the body without affecting other parts. d. guarantees that the timing of gene expression is the same in all parts of a developing embryo. e. allows organisms to be built up one module at a time. 6. Organisms often respond developmentally to regularly occurring environmental signals that accurately predict future conditions by a. stopping development until the signal changes. b. altering their development such that the resulting adult is adapted to the future environment. c. altering their development such that the resulting adult can produce offspring adapted to the future environment. d. producing new mutants. e. developing normally because the predicted conditions may not last long. 7. The phenomenon wherein organisms change the relative time of appearance and rate of development of characters is called a. heterochrony. b. developmental plasticity. c. adaptation. d. modularity. e. mutation. 8. Daphnia with large helmets are more difficult for some predators to capture and eat, but not all Daphnia produce large helmets because a. individuals with large helmets cannot feed efficiently. b. individuals with large helmets have trouble mating. c. individuals with large helmets produce fewer eggs than individuals with small helmets. d. individuals with large helmets become ensnared in vegetation. e. some individuals lack the genes that govern helmet formation. 9. Which of the following is not an important characteristic of plants that affects their development? a. Most plants are sessile. b. Plant cells do not move relative to one another during development. c. Plants produce meristems regularly as long as they grow. d. Plants have great developmental plasticity. e. Plants set aside germ cells early during embryonic development. 10. Which of the following plant structures does not change in response to the conditions under which a plant grows? a. Roots b. Seeds c. Leaves d. Stems e. Branches For Discussion 1. What components of environmental influences on development would likely be missed if investigations were confined to simple organisms? 2. A spadefoot toad tadpole that develops in a rapidly drying pond is likely to eat many of its brothers and sisters. How can eating its siblings, which share half of an individual s genes, be favored by natural selection? 3. If evolutionary novelties can result from rather simple changes in the timing of expression of a few genes, why have such novelties arisen relatively infrequently during evolution? 4. Francois Jacob claimed that evolution was more like tinkering than engineering. Does the observation that developmental genes have changed little over evolutionary time support his assertion? Why? 5. We have learned in this chapter that plants and animals share many of the genes that regulate development. What are the implications of this observation for the ways in which humans can respond to the adverse effects of the many substances we release into the environment that cause developmental abnormalities in plants and animals? What kinds of substances are most likely to have such effects? Why?

13 LIFE ESSAY What are the moral issues surrounding stem cell therapy? - by Bonnie Steinbock - There are two kind of stem cells: adult and embryonic. All stem cells have potential medical uses, but embryonic stem (ES) cells are thought by scientists to have especially great medical potential because they have the ability to become any kind of cell in the body. Stem cells may one day play an important role in the treatment of such diseases as Parkinson s, Alzheimer s, osteoporosis, macular degeneration, cancer, diabetes, and heart disease, as well as in the treatment of burns and spinal cord injury. While the use of adult stem cells in research does not raise moral questions, ES cell research does because ES cells are derived from early embryos (blastocysts), and thus involves the destruction of an embryo. ES cells can be derived from embryos created specifically for research or from embryos created originally for infertility treatment but no longer needed ( spare embryos). Some people think it is not permissible to create embryos for research, but it is morally permissible to use (and destroy) embryos that would be discarded anyway. Others think it is wrong to use either created or spare embryos in research; still others think it is permissible to use embryos in research regardless of their original intended use. How people think about ES cell research depends largely on their views about the moral status of human embryos. Three views on this have different implications for embryo research: 1. Embryos are human subjects, entitled to all the protection of any other human subjects. This view rules out all embryo research that harms or kills embryos. 2. Embryos, while biologically human, are not human beings in a moral sense. What makes someone a human being in a moral sense that is, a possessor of rights, a full member of the moral community; in short, a person is not the species to which it belongs or the number of chromosomes it has, but rather whether it possesses the morally significant characteristics that human beings typically have sentience, consciousness, self-consciousness, rationality, and the like. Embryos have none of these characteristics and therefore research on embryos is morally permissible. 3. Embryos, while not persons, nevertheless deserve special respect and serious moral consideration as a developing form of human life. This third view, a compromise between the first two views, allows for some embryo research, under carefully controlled conditions. Critics maintain that the third view is incoherent, that it is impossible to show respect to embryos if one is planning to kill them. The challenge for those who advocate the third view is to give content to the notion of respect for embryos. First, it is important to determine what respect for embryos might mean in contrast to respect for persons. Respect for persons, as Kant instructs us, means never treating persons as mere means to our ends, but always treating them as ends in themselves. This means that we must take seriously other people s ends their plans and goals and not just our own. This kind of respect is limited to beings who can have plans and goals, and thus is not appropriate to early embryos. Embryos lack any sort of consciousness or awareness. But even if embryos cannot be treated with the respect due to persons, there may still be moral reasons to treat them in some ways and not others. It is Bonnie Steinbock received her Ph.D.in philosophy from the University of California, Berkeley. She has taught at the University at Albany since 1977, where she is a Full Professor and currently Chair of the Department of Philosophy. Her areas of specialization within bioethics include reproduction and genetics. She is the author of Life Before Birth:The Moral and Legal Status of Embryos and Fetuses,numerous articles, and the editor or co-editor of several anthologies, including the sixth edition of Ethical Issues in Modern Medicine. not only persons, or even sentient beings such as animals, that have moral significance. Plants, wilderness areas, entire species, or ecosystems may also deserve respect and protection. The potential of embryos to become human gives us a reason to treat them with more respect than other bodily tissues, even if it is not enough to endow embryos with full moral status and full moral rights. What, then, does respect for embryos require? The third view does not rule out embryo research any more than respect for the dead precludes autopsies. Respect for embryos rules out frivolous or trivial uses, such as using human embryos in high school science classes, to test the safety of cosmetics, or to create jewelry. These are situations in which there is no pressing need to use human embryos; in such cases their use displays contempt rather than respect for human life. However, respect for human life does not rule out significant medical research that could save many lives or contribute to other worthy medical goals such as improving fertility treatment, reducing pain, or preventing disability. Discussion Questions 1. Are embryos persons? On what do you base your view? 2. What is the created/spare distinction? Do you think it has moral significance? 3. Is it consistent to allow abortion but ban ES cell research? Web Links National Information Resources on Ethics and Human Genetics nirehg/index.html Yahoo! Biology: Science: Biomedical Ethics Medical Ethics Science/Biology/Biomedical_Ethics/ Center for the Study of Bioethics Bioethics Resources on the Web National Institute of Health bioethics/index.html