21 Development and Evolutionary Change

21 Introduction Evolution and Development Regulatory Genes and Modularity: Modifying Morphology Plant Development and Evolution Environmental Influences on Developmental Patterns Learning: A Modification of Development

21 Introduction Fish that can change their sex in response to their social environment, such as anemonefish, demonstrate that an organism’s development is not determined entirely by its genes. The phenotypes of adult organisms are the result of complex interactions between basic genes, gene products, and the environment.

21 Evolution and Development Charles Darwin’s idea of characterizing evolution as “descent with modification” led to the recognition that the results of evolution could be visualized as a “tree of life.” He explained similarities among organisms by their descent from a common ancestor. Differences among organisms were explained as the result of natural selection, which adapted them to different environments.

21 Evolution and Development Darwin recognized and showed that similarities among embryos could be used to infer the relationships among groups of organisms. Using similarities in larval forms as a basis, Darwin was able to conclude that barnacles are crustaceans.

Figure 21.1 Similarities In Early Developmental Stages Can Be Used to Infer Relationships

21 Evolution and Development Late in the twentieth century, the fields of genetics and embryology came 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. Many of the genes regulating development are highly conserved, meaning their sequences have changed very little throughout the evolution of multicellular organisms.

21 Evolution and Development Many of the genes that regulate the development of very different animal species are remarkably similar. For example, many of the same genes are involved in the development of the compound eyes of fruit flies and the camera-like eyes of house mice. The genes involved in eye development in these two species are so similar that the fruit fly cell that normally develops into part of a leg will form an eye when a mouse Pax6 gene is expressed in it.

Figure 21.2 The Mouse Pax6 Gene Causes Eye Development in Drosophila

21 Evolution and Development The same set of homeobox genes provides the positional information along the anterior–posterior axis of the body in both human and insect embryos. For example, the Drosophila gap genes ems, tll, and otd, as well as the homologous genes of vertebrates are expressed in the anterior regions of the brain.

Figure 21.3 Genes Show Similar Expression Patterns

21 Evolution and Development Mutations of genes involved in development can result in abnormal differentiation during development. The bithorax mutation in insects, for example, results in the development of two sets of forewings instead of one pair. When the expression of certain vertebrate Hox genes is altered, vertebrae that normally develop into lumbar vertebrae instead develop instead into thoracic vertebrae.

Figure 21.4 Altering Homeobox Genes Changes Morphology

21 Evolution and Development The enormous amount of variation of morphological forms found in animals is underlain by a common set of instructions that have been conserved in thousands of species. The vast differences in morphological form that result from similar genetic instructions means that these instructions alone cannot be entirely responsible for an organism’s morphology.

21 Regulatory Genes and Modularity: Modifying Morphology Developing embryos exhibit modularity—they are made up of self-contained units that can be changed independently of the other units, or modules, that compose the organism. There are two ways in which changes in genes that regulate development can lead to important morphological changes:  Mutations in genes that regulate developmental processes  Changes in the time or place of expression of developmental regulatory genes The modular nature of most organisms makes both of these pathways of evolution easier.

21 Regulatory Genes and Modularity: Modifying Morphology Insects provide examples of how mutations in genes that regulate segmentation can lead to the evolution of morphological changes. For example, the homeotic gene Ultrabithorax (Ubx), which is found in all organisms. The insect Ubx gene has a mutation not found in other arthropods. The Ubx protein produced from this mutated gene is expressed in the abdomen of insects, where it represses the expression of the distal-less (dll) gene, which is essential for leg formation. As a result of the Ubx repression of the dll gene, insects do not form legs on their abdomens.

Figure 21.5 A Mutation Changed the Number of Legs in Insects

21 Regulatory Genes and Modularity: Modifying Morphology The evolution of webbed feet in ducks provides an example of an altered spatial expression pattern of a regulatory gene. A gene encoding a protein called bone morphogenetic protein 4 (BMP4) is expressed in the spaces between the developing bones of the toes and instructs the cells in those spaces to undergo apoptosis, destroying the webbing between the toes. Ducks express a BMP inhibitor protein called Gremlin in their webbing cells. This protein prevents the BMP4 protein from signaling for cell death in the webbing, resulting in a webbed foot.

Figure 21.6 Changes in gremlin Expression Correlate with Changes in Hindlimb Structure

Figure 21.7 Changing the Form of an Appendage

21 Regulatory Genes and Modularity: Modifying Morphology Modularity allows the relative timing of two different developmental processes to shift independently of one another. This process is known as heterochrony and has been widely studied in salamanders. Two species of Bolitoglossa illustrate heterochrony. The webbing between the feet of most salamander species disappears as the animals mature. If expression of genes that dissolve the webbing is slowed, the digits don’t grow, and “juvenile” webbed feet result. These feet can act like suction cups, opening an arboreal way of life.

Figure 21.8 Heterochrony Created an Arboreal Salamander

21 Regulatory Genes and Modularity: Modifying Morphology Modularity also allows structural changes to evolve via gene duplication. If a gene is duplicated, the new copy can evolve a new function without disrupting the organism as long the other copy is performing its original function.

21 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. The sequencing of the complete genome of the thale cress, Arabidopsis thaliana, has provided much of this information. About 1,500 of the nearly 26,000 Arabidopsis genes code for transcription factors. Over half of the known families of transcription factors are found in all eukaryotes, but many others are found only in plants.

21 Plant Development and Evolution Plants and animals share many regulatory genes, but plants differ from animals in important ways:  Plant cells do not move relative to one another. Changes in the shape of a developing plant result from cell proliferation and elongation.  Future reproductive cells are not set aside early during plant development. Plants produce clusters of undifferentiated, actively dividing cells called meristems throughout their lives.  Plants have tremendous developmental plasticity. Plants can change their development in response to environmental conditions.

21 Plant Development and Evolution Members of the MADS box and homeobox families of genes encode transcription factors that regulate developmental processes in both plants and animals. Plants and animals share many of the genes that regulate their development, even though they have been evolving separately for a long time. This is in part due to their modular construction which allows different parts of their bodies to change independently of one another.

21 Plant Development and Evolution Plants have greater developmental plasticity than animals do because plasticity is especially valuable for a sessile organism. The combination of repeated production of meristems and developmental plasticity compensates for being sessile.

21 Environmental Influences on Developmental Patterns The idea that the environment plays an important role in the development of organisms was downplayed until recently. Developmental biologists tended to study small organisms that develop rapidly and do not change dramatically under controlled conditions. It is now known that the development of many organisms is very sensitive to environmental conditions. A single genotype may encode a range of phenotypes under different environmental conditions.

21 Environmental Influences on Developmental Patterns Signals from the environment can be divided into two major types:  Environmental signals that are accurate predictors of future conditions. It is expected that the developmental processes of organisms respond adaptively to these signals.  Environmental signals that are poorly correlated with future conditions. Organisms are unlikely to respond to these signals.

21 Environmental Influences on Developmental Patterns Developing organisms respond to signals such as day length, temperature, and precipitation in such a way that the adults they become are adapted to the predicted conditions. The West African butterfly Bicyclus anynana has a dry-season form and a wet-season form with different wing coloration. The temperatures experienced during pupation determine which form of adult butterfly will be produced. Temperature influences the expression of the distal-less gene.

Figure 21.9 Development of Eyespots in Bicyclus anynana Responds to Temperature

21 Environmental Influences on Developmental Patterns The moth Nemoria arizonaria provides another example of developmental plasticity in response to seasonal changes. The spring larvae of this moth feed on and resemble oak flowers; the summer larvae feed on oak leaves and resemble small oak branches. Spring caterpillars have been experimentally converted to summer caterpillars by feeding them oak leaves. A chemical in the oak leaves probably induces them to develop into the twiglike summer form.

Figure The Spring and Summer Forms of a Caterpillar Differ

21 Environmental Influences on Developmental Patterns Some organisms need help from another species to complete their development. For example, house mice raised in microbe-free environments do not have the bacteria that normally colonize their gut. These gut bacteria induce gene expression in the mouse intestine, which is essential for normal capillary development.

21 Environmental Influences on Developmental Patterns Many changes to an organism’s environment are not as certain as signals such as day length or wet- and dry-seasons. Despite this uncertainty, if the changes have occurred frequently during the evolution of a species, developmental plasticity may allow individuals to respond to them. The presence or absence of active predators is an example of one of these uncertain environmental signals.

21 Environmental Influences on Developmental Patterns Water fleas (Daphnia), for example, increase the size of the “helmets” on the top of their heads when they encounter the predatory larvae of the fly Chaoborus. Helmet induction occurs if the Daphnia are exposed to water in which the fly larvae have been swimming. Offspring that are developing in the abdomens of mothers with induced large helmets are born with large helmets. The tradeoff for this defensive advantage is that Daphnia with large helmets produce fewer eggs.

Figure Predator-Induced Developmental Plasticity in Daphnia

21 Environmental Influences on Developmental Patterns Tadpoles of the spadefoot toad can respond developmentally if their pond begins to dry up while they are growing. Some of the tadpoles respond to crowding in a shrinking pond by developing a wider mouth and powerful jaw muscles. These tadpoles complete their development rapidly before the pond dries up by eating other tadpoles.

21 Environmental Influences on Developmental Patterns Plants respond developmentally to light availability. In low light conditions, plant cells elongate so that the plants become spindly and are more likely to reach a patch of brighter light than if they were to remain compact. Because they have meristems, plants can continue to respond to light as long as they grow.

Figure Light Seekers

21 Environmental Influences on Developmental Patterns Organisms generally ignore environmental signals that are poorly correlated with future conditions. Plants, for example, produce seeds that will germinate in future years with different and unknowable conditions. Plant seed sizes remain relatively constant in spite of changing environmental conditions. Seed size is adjusted to the average conditions encountered by plants over many generations.

Figure Seed Production

21 Environmental Influences on Developmental Patterns Organisms cannot be expected to have evolved appropriate responses to environmental signals that they have not encountered before. This is an important problem because human societies have changed the environment in so many ways. One way humans change the environment is through the release of new chemical compounds. Understanding how chemicals affect development is important because it may help in the development of less harmful substitutes.

21 Learning: A Modification of Development Learning allows an individual to adjust its behavior to the physical, biological, and social environment in which it matures. Learning is especially important in species with complex social structures, in which individuals must learn the identities and characteristics of their associates and adjust their behavior accordingly. The field of evolutionary developmental biology is generating many new insights with which to understand the evolution of life.