Evolutionary Biology PDF

PINK NUDIBRANCH (Hypeselodoris bullock) - group: Marine mollusk - unususal shapes and Bright color - poisonous; to protect itself from predator. - adaptation (theory of evolution by natural selection.  1...

PINK NUDIBRANCH (Hypeselodoris bullock) - group: Marine mollusk - unususal shapes and Bright color - poisonous; to protect itself from predator. - adaptation (theory of evolution by natural selection.  1 Evolutionary Biology In February 2014, in the West Africa country Sierra Leone, the first cases were reported of the horrifying disease caused by Ebola virus. It rapidly spread to Liberia and Guinea, and within 15 months it had stricken more than 26,000 people and killed more than 11,000. Among the first questions epidemiologists ask about a new or resurgent infectious disease are where it originated and by what paths it spread. Within 7 months after the start of the Ebola outbreak, a team of health scientists, molecu- lar biologists, and evolutionary biologists had an answer. Based on an evolu- tionary analysis of the viral genomes from several patients, the researchers con- cluded that the West Africa virus had almost certainly spread from central Africa about a decade earlier, and that the 2014 outbreak originated from a single person who contracted the virus from another host species, probably a bat. This was an important point, because it indicated that although the virus is readily transmitted from one person to another, it is only rarely contracted by humans from other species. This was by no means the first time evolutionary methods had been used to trace the origin of an infectious disease. This approach has been routine ever since the origin of the human immunodeficiency virus (HIV), which causes AIDS, was determined in 1989. Two distinct HIVs (HIV-1 and HIV-2) infect humans; the pandemic is caused by HIV-1. Both HIVs are lentiviruses, a group of retrovi- ruses that infect diverse mammals. In monkeys and other primates, the viruses are called simian immunodeficiency viruses, or SIVs (FIGURE 1.1). An evolution- ary analysis showed that HIV-2 recently evolved from an SIV carried by sooty This pink nudibranch (Hypselodoris bullocki) is a spectacular example of a group of marine mollusks renowned for their unusual shapes and bright coloration. Many nu- dibranchs contain toxins as a defense against predation and their unusual colors may be an adaptation that warns potential predators not to eat them. The only scientific explanation of such adaptations is the theory of evolution by natural selection. 4    CHAPTER 1 (A) FIGURE 1.1 (A) Structural model of a human im- munodeficiency virus (HIV). (B) The sooty mangabey (Cercopithecus atys) and (C) the chimpanzee (Pan troglodytes) are the sources of two forms of HIV. (B) (C) mangabey monkeys, and that HIV-1 evolved from SIVcpz, the virus that infects wild chimpanzees (FIGURE 1.2) [9, 25]. The evolutionary analysis showed, moreover, that HIV-1 entered the human population near the beginning of the twentieth century, decades before it spread beyond Africa. It is thought that humans became infected with SIVs by contact with the blood of chimpanzees and mangabeys that they killed for food. These viruses do not have a fossil record, so how could biologists infer their evolution and spread? They used methods that have been developed to recon- struct evolutionary history, and that are based on understanding the processes of evolutionary change. Understanding the processes of evolution is highly relevant to human health. For example, the first drug approved to treat HIV-infected people was AZT, in 1987. Within a few years, however, AZT failed to prevent many infected patients from developing AIDS, and it has been necessary to develop other drugs. What happened? Populations of HIV had adapted to AZT by evolving resistance. Ever since the first antibiotic—penicillin—came into use, bacteria and other patho- genic microbes have rapidly evolved resistance to every antibiotic that has been widely used (FIGURE 1.3) [20, 22]. Staphylococcus aureus, a bacterium that causes many infections in surgical patients, has evolved resistance to a vast array of antibiotics, starting with penicillin and working its way through many others. Drug-resistant strains of Neisseria gonorrheae, the bacterium that causes gonor- rhea, have steadily increased in abundance, and many strains of the tuberculosis, pneumonia, and cholera bacteria are highly resistant to antibiotics. Throughout the tropics, the microorganism that causes malaria is now resistant to chloro- quine and is becoming resistant to other drugs as well. Worldwide, more than Futuyma Kirkpatrick Evolution, 4e a half million people die yearly from drug-resistant infections. The evolution of Sinauer Associates antibiotic resistance is a major Evolution4e_01.01.ai crisis Date in public health [3, 22]. 12-06-2016  Evolutionary Biology   5 HIV-1 human FIGURE 1.2 A phylogenetic tree showing SIVcpz chimpanzee the history by which various immunodefi- ciency viruses have evolved. Time runs from SIVgor gorilla left to right, and the common ancestor of all the viruses is at the left (the “root” of the SIVcpz chimpanzee tree). One lineage gave rise to the viruses that infect primates: lemurs, monkeys, and apes. These simian immunodeficiency viruses SIVmnd mandrill (SIVs) are labeled with abbreviations of the names of the infected species (e.g., SIVcpz in SIVagm Afr. green monkey chimpanzee). The human immunodeficiency viruses HIV-2 and HIV-1 arose from SIVs that HIV-2 human infected monkeys and chimpanzees, respec- tively. (After.) SIVsmm sooty mangabey Viral replication: 1.) lysogenic and 2.) lytic cycle - 1.) virus sneak to the host's DNA; 2.) SIVcol colobus monkey virus quickly take over the host cell, make many copies, break the cell, and infect other Lemur cell. Cat Apes - carrier Human - shows symptoms (host) Rabbit ex. Swine flu: not affected ung human sa pig mataas ung mortality rate Horse virulence - how the virus cause symptoms Almost every hospital in the world treats casualties in this battle against changing opponents, but as the use of antibiotics increases, so does the incidence of bacteria that are resistant to those antibiotics; thus any gains made are almost as quickly lost (see Figure 1.3). Why is this happening? Do the drugs cause drug- resistant mutations in the bacteria’s genes? Do the mutations occur even without - The body develop resistance in antibiotic because of the misusage of the antibiotics. (A) - Must follow the dosage (B) 1.4 14 30 Prevalence of resistant bacteria (%) Number of doses prescribed (millions) Third-generation 12 Percentage of isolates resistant 1.3 25 Measure of drug use (volume) 100 cephalosporin resistance Drug use 10 80 1.2 20 8 60 1.1 15 Prevalence 6 Carbapenem of resistant 1.0 prescriptions 10 40 bacteria 4 20 0.9 Carbapenem 5 2 resistance 0 0.8 0 0 1978 1980 1982 1984 1986 1988 1990 1992 2000 2002 2004 2006 2008 2010 Year Year FIGURE 1.3 Evolution of drug resistance. (A) An increase tions in young children. (B) Resistance of the pneumonia- in the use of a penicillin-like antibiotic in a community in causing bacterium Klebsiella pneumoniae to cephalosporin Finland between 1978 and 1993 was matched by a dramatic and carbapenem antibiotics has recently begun to increase increase Futuyma in the percentage Kirkpatrick Evolution, 4eof antibiotic-resistant isolates of in the United States. The use of carbapenems approximately the bacterium Sinauer AssociatesMoraxella catarrhalisis from middle-ear infec- doubled during the period shown. (A after ; B after.) Troutt Visual Services Qu: Should part (B) y-axis label be worded similarly to (A)? For example: “Prevalence of resistant isolates (%)” Evolution4e_01.02.ai Date 10-31-2016 12-06-16 6    CHAPTER 1 exposure to drugs—that is, are they present in unexposed bacterial populations? Do the mutations spread among different species of bacteria? Can the evolution of resistance be prevented by using lower doses of drugs? Higher doses? Combi- nations of different drugs? Microbial adaptation to drugs is the same, in principle, as the countless adap- tations of every species to its environment, so it is very familiar to evolutionary biologists. The principles and methods of evolutionary biology have provided some answers to these questions about antibiotic resistance, and have shed light on many other problems that affect society. Evolutionary biologists have studied the evolution of insecticide resistance in disease-carrying and crop-destroying insects. They have helped devise methods of nonchemical pest control and have laid the foundations for transferring genetic resistance to diseases and insects from wild plants to crop plants. Evolutionary principles and knowledge are being used in biotechnology to design new drugs and other useful products, and in medical genetics to identify and analyze inherited diseases as well as variation in susceptibility to infectious diseases. In the fields of computer science and artifi- cial intelligence, “evolutionary computation” uses principles taken directly from evolutionary theory to solve mathematically difficult practical problems, such as constructing complex timetables and processing radar data. The importance of evolutionary biology goes far beyond its practical uses. An evolutionary framework provides answers to many questions about ourselves. How do we account for human variation—the fact that almost everyone is genetically and phenotypically unique? What accounts for behavioral differences between men and women? How did exquisitely complex, useful features such as our hands and our eyes come to exist? What about apparently useless or even potentially harmful characteristics such as our wisdom teeth and appendix? Why do we age, senesce, and eventually die? Evolution raises still larger questions. As soon as Darwin published On the Origin of Species in 1859, the evolutionary perspective was perceived to bear on long-standing questions in philosophy. If humans, with all their mental and emotional complexity, originated by natural processes, where do ethics and moral precepts find a foundation and origin? What, if anything, does evolution imply about the meaning and purpose of life? Must one choose between evolution and religious belief? “Nothing in Biology Makes Sense except in the Light of Evolution” If you suppose that scientists study evolution by analyzing fossils, you are right— but as the analyses of infectious diseases show, students of evolution also employ many other approaches and address a wide range of questions. Evolutionary biology is concerned with explaining and understanding the diversity of living things and their characteristics: what has been the history that produced this diversity, and what have been the causes of this history? Some evolutionary scientists try to elucidate the history of viruses, how they became capable of infecting diverse species of animals, and how antibiotic resistance evolves. Others ask similar questions about the ori- gin of humans and human characteristics—or of mammals, plants, beetles, or dino- saurs. And because all features of all organisms have evolved, evolutionary biologists study the evolution of DNA sequences, proteins, biochemical pathways, embryologi- cal development, anatomical features, behaviors, life histories, interactions among different species: all of biology. Facing such an overwhelming profusion of subjects, evolutionary scientists aim to develop broad principles and to document common patterns of evolution—to arrive at general principles that apply to diverse organisms  Evolutionary Biology   7 FIGURE 1.4 The song of a male marsh warbler Marsh warbler 8 (Acrocephalus palustris) is much more complex than the song of a male grasshopper warbler (Locustella naevia), which is a simple buzz. kHz 4 The sonograms (diagrams of the song) show frequency in relation to time. The song nucleus 0 0 1 in the brain is larger in the marsh warbler than Time (s) in the grasshopper warbler. Female marsh war- blers prefer males with more complex songs. The proximate causes of the song difference include the brain structure; the ultimate causes Grasshopper warbler include natural selection owing to the reproduc- 8 tive success of males whose songs attract more females. (Sonograms from.) kHz 4 Bioacustics - a specific species will emit a 0 specific sounds that only its species can 0 1 recognize. Time (s) and diverse kinds of characteristics. Most of this book attempts to convey these gen- eral principles, although we illustrate the principles with studies of particular organ- isms and characteristics. Evolutionary biology extends and amplifies the explanation of biological phe- nomena. It complements studies of the proximate causes (immediate, mechani- cal causes) of biological phenomena—the subject of cell biology, neurobiology, and many other biological disciplines—with analysis of the ultimate causes of those phenomena: their historical causes, especially the action of natural selec- tion. If we ask what causes a male bird to sing, the proximate causes include the action of testosterone or other hormones, the structure and action of the singing apparatus (syrinx), and the operation of certain centers in the brain (FIGURE 1.4). The ultimate causes lie in the history of events that led to the evolution of singing in the bird’s remote ancestors. For example, past individuals whose genes inclined them to sing may have been more successful in attracting females or in driving away competing males, and thus may have transmitted their genes to more descendants than did their less vocal competitors. Proximate and ulti- mate explanations may interact , and together provide more complete under- standing than either does alone. As the great evolutionary biologist Theodosius Dobzhansky wrote, “Nothing in biology makes sense except in the light of evolution.” What Is Evolution? Is It Fact or Theory? The word “evolution” comes from the Latin evolvere, “to unfold or unroll”—to reveal or manifest hidden potentialities. Today “evolution” has come to mean, simply, “change.” But changes in individual organisms, such as those that transpire in devel- opment (ontogeny) are not considered evolution. Biological (or organic) evolution is inherited change in the properties of groups of organisms over the course of generations. As Darwin elegantly phrased it, evolution is descent with modification. As the HIV and SIV viruses illustrate, a single group, or population, of organ- isms may be modified over the course of time (e.g., becoming drug-resistant). A population may become subdivided, so that several populations are descended from a common ancestral population. If different changes transpire in the several Futuyma Kirkpatrick Evolution, 4e Sinauer Associates Troutt Visual Services Evolution4e_01.04.ai Date 10-31-2016 12-06-16 8    CHAPTER 1 populations, the populations diverge —that is, they become different from each other (e.g., as the various HIVs and SIVs have done). Is evolution a fact, a theory, or a hypothesis? Biologists often speak of the “theory of evolution,” but they usually mean by that something quite different from what most nonscientists understand by that phrase. Biologists talk about the “theory of evolution” in the same way that physicists talk about the “theory of gravitation.” Scientists are as confident about the reality of evolution as they are of the reality of gravity. In science, a hypothesis is an informed conjecture or statement of what might be true. Most philosophers (and scientists) hold that we do not know anything with absolute certainty. What we call “facts” are in some cases simple, confirmed observations; in other cases, a “fact” is a hypothesis that has acquired so much supporting evidence that we act as if it is true. A hypothesis may be poorly sup- ported at first, but it can gain support to the point that it is effectively a fact. For Copernicus, the revolution of Earth around the Sun was a hypothesis with mod- est support; for us, this hypothesis has such strong support that we consider it a fact. Occasionally, an accepted “fact” may need to be revised in the face of new evidence; for example, humans have 46 chromosomes, not 48 as once thought. In everyday use, “theory” refers to an unsupported speculation. Like many words, however, this term has a different meaning in science. Strictly speaking, a scientific theory is a comprehensive, coherent body of interconnected statements, based on reasoning and evidence, that explain some aspect of nature—usually many aspects. Thus atomic theory, quantum theory, and the theory of plate tec- tonics are elaborate schemes of interconnected ideas, strongly supported by evi- dence, that account for a great variety of phenomena. “Theory” is a term of honor in science; the greatest accomplishment a scientist can aspire to is to develop a valid, successful new theory. In The Origin of Species, Darwin propounded two major hypotheses: that organ- isms have descended, with modification, from common ancestors; and that the chief cause of modification is natural selection acting on hereditary variation. Darwin provided abundant evidence for descent with modification; since then, hundreds of thousands of observations from paleontology, geographic distri- butions of species, comparative anatomy, embryology, genetics, biochemistry, and molecular biology have confirmed that all known species are related to one another through a history of common ancestry. Thus the hypothesis of descent with modification from common ancestors has long had the status of a scientific fact. (We will describe some of the evidence in Chapters 2 and 22.) The explanation of how modification occurs and how ancestors give rise to diverse descendants constitutes the scientific theory of evolution. We now know that Darwin’s hypothesis that evolution occurs by natural selection acting on hereditary variation was correct. We also know that there are more causes of evolution than Darwin realized and that natural selection and hereditary varia- tion are more complex than he imagined. A body of ideas about the causes of evolution, including mutation, recombination, gene flow, isolation, random genetic drift, the several forms of natural selection, and other factors constitutes our current theory of evolution, or “evolutionary theory.” Like all theories in science, it is a work in progress, for we do not entirely know the causes of all of evolution, or of all the biological phenomena that evolutionary biology will have to explain. In evolutionary biology, as in every other scientific discipline, there are “core” principles that have withstood skeptical challenges and are highly unlikely to require revision, and there are “frontier” areas in which research actively continues. Some widely held ideas about frontier subjects may prove to  Evolutionary Biology   9 be wrong, but the uncertainty at the frontier does not undermine the core. The main tenets of evolutionary theory—descent with modification from a common ancestor, in part caused by natural selection—are so well supported that almost all biologists confidently accept evolutionary theory as the foundation of the science of life. The Evolution of Evolutionary Biology That the past is often the key to the present may be a cliché, but it happens to be true. Just as evolutionary history has shaped today’s organisms, and just as social and political history is the key to understanding today’s nations and conflicts, so the con- tent of any science or other intellectual discipline cannot be fully understood without reference to its history. Before Darwin Darwin’s theory of biological evolution is one of the most revolutionary ideas in Western thought, perhaps rivaled only by Newton’s and Einstein’s theories of phys- ics. It profoundly challenged the prevailing worldview, which had originated largely with Plato and Aristotle, who developed the notion that species have fixed proper- ties. Later, Christians interpreted the biblical account of Genesis literally and con- cluded that each species had been created individually by God in the same form it has today. (This belief is known as “special creation.”) Christian theologians and philosophers argued that since existence is good and God’s benevolence is complete, He must have bestowed existence on every creature of which He could conceive. Because order is superior to disorder, God’s creation must follow a plan: specifically, a gradation from inanimate objects and barely animate forms of life through plants and invertebrates and up through ever “higher” forms of life. Humankind, being both physical and spiritual in nature, formed the link between animals and angels. This “Great Chain of Being,” or scala naturae (the scale, or ladder, of nature), must be permanent and unchanging, since change would imply that there had been imper- fection in the original creation. As late as the nineteenth century, natural history was justified partly as a way to reveal the plan of creation so that we might appreciate God’s wisdom. Carolus Linnaeus (1707–1778), who established the framework of modern taxonomy in his Systema Naturae (1735), won worldwide fame for his exhaustive classifica- tion of plants and animals, undertaken in the hope of discovering the pattern of the creation. Linnaeus classified “related” species into genera, “related” genera into orders, and so on. To him, “relatedness” meant propinquity in the Creator’s design. Belief in the literal truth of the biblical story of creation started to give way in the eighteenth century, when a philosophical movement called the Enlighten- ment, largely inspired by Newton’s explanations of physical phenomena, adopted reason as the major basis of authority and marked the emergence of science. The foundations for evolutionary thought were laid by astronomers, who developed theories of the origin of stars and planets, and by geologists, who amassed evi- dence that Earth had undergone profound changes, that it had been populated by many creatures now extinct, and that it was very old. The geologists James Hutton and Charles Lyell expounded the principle of uniformitarianism, holding that the same processes operated in the past as in the present and that the data of geology should therefore be explained by causes that we can now observe. Darwin was greatly influenced by Lyell’s teachings, and he adopted uniformitari- anism in his thinking about evolution. Carolus Linnaeus - binomial nomenclature (Genus specific ephithet) 10    CHAPTER 1 (A) Lamarck’s hypothesis (B) Darwin’s hypothesis Complexity Form Time Time FIGURE 1.5 Lamarck’s and Darwin’s hypotheses of the history of evolution. (A) Under Lamarck’s hypothesis, life has originated many times (the red dots). Each lineage that descends from one of these origins becomes more complex. Thus, organisms range from recently originated, simple forms of life to older, more complex forms. (B) Dar- win’s theory of descent with modification, represented by a phylogenetic tree. From a single ancestor (the red dot), different lineages arise by speciating (splitting) from ex- isting lineages. Some (such as the more central lineages) may undergo less modifica- tion from the ancestral condition than others. Darwin supposed that species become different from each other in various features (“form”), not necessarily becoming more complex. (A after.) In the eighteenth century, several French philosophers and naturalists sug- gested that species had arisen by natural causes. The most significant pre-Dar- winian evolutionary hypothesis was proposed by the Chevalier de Lamarck in his Philosophie Q: Does Zoologique Darwin’s version (1809). need any Lamarck hypothesized that different organisms red nodes along the curvy branches? originated separately by spontaneous generation from nonliving matter, starting at the bottom of the chain of being. A “nervous fluid” acts within each species, he said, causing it to progress up the chain. Species originated at different times, so we now see a hierarchy of species because they differ in age (FIGURE 1.5A). Lamarck argued that species differ from one another because they have differ- ent needs, and so use certain of their organs and appendages more than others. Just as muscles become strengthened by work, more strongly exercised organs attract and become enlarged by the “nervous fluid.” Lamarck, like most people at the time, believed that such alterations, acquired during an individual’s lifetime, are inherited—a principle called inheritance of acquired characteristics. The the- ory of evolution based on this principle is called Lamarckism. In the most famous example of Lamarck’s theory, giraffes must have stretched their necks to reach foliage above them, and so their necks were lengthened. The longer necks were Jean-Baptiste Pierre Antoine de inherited, and over the course of generations, this process was repeated and their Monet, Chevalier de Lamarck necks got longer and longer. This could happen to any and all giraffes, so the entire species could have acquired longer necks because it was composed of indi- vidual organisms that changed during their lifetimes (FIGURE 1.6A). Lamarck’s ideas of how evolution works were wrong, but he deserves credit for being the first to advance a coherent and testable theory of evolution. Charles Darwin Charles Robert Darwin (February 12, 1809–April 19, 1882) was the son of an Eng- lish physician. He briefly studied medicine in Edinburgh, then turned to studying for a career in the clergy at Cambridge University. He believed in the literal truth of the Bible as a young man. He was passionately interested in natural history. In 1831, at the age of 22, his life was forever changed when he was invited to serve as Futuyma Kirkpatrick Evolution, 4e Sinauer Associates Troutt Visual Services Evolution4e_01.05.ai Date 10-31-2016  Evolutionary Biology   11 (A) Lamarck’s hypothesis FIGURE 1.6 Contrast between Lamarck’s Generation 1 Generation 2 and Darwin’s hypotheses for how charac- Young adults Older adults Young adults teristics evolve, shown across two genera- tions. (A) Under Lamarck’s hypothesis, traits change within the lifetime of individuals because of their needs, illustrated here by giraffes that need longer necks to reach high leaves. Changes that are acquired during this generation are passed on to the next generation. (B) Under Darwin’s hypothesis, there is variation among individuals at the start of each generation. Individuals with certain traits (e.g., a longer neck) have a greater chance of surviving. The variation is inherited, so survivors pass (B) Darwin’s hypothesis on their traits to the next generation. Dar- win was right, but about 50 years would Generation 1 Generation 2 pass before scientists would understand Young adults Surviving adults Young adults how the inherited variations arise. a naturalist and captain’s companion on the British Navy ship h.m.s. Beagle, tasked with charting the coast of South America. The voyage of the Beagle lasted from December 27, 1831, to October 2, 1836. The ship spent several years traveling along the coast of South America, where Darwin observed the natural history of the Brazilian rainforest and the Argentine pampas, then stopped in the Galápagos Islands, which lie on the equator off the coast of Ecuador. In the course of the voyage, Darwin became an accomplished naturalist, collected specimens, made innumerable geological and biological observations, and conceived a new (and correct) theory about the formation of coral atolls. Soon after Darwin returned, the ornithologist John Gould pointed out that Darwin’s specimens of mockingbirds from the Galápagos Islands were so differ- ent from one island to another that they represented different species (FIGURE 1.7). Darwin then recalled that the giant tortoises, too, differed from one island to the next (FIGURE 1.8). These facts, and the similarities between fossil and living mammals that he had found in South America, triggered his conviction that dif- ferent species had evolved from common ancestors. Darwin’s comfortable finances enabled him to devote the rest of his life exclu- sively to his scientific work (although he was chronically ill for most of his life after the voyage). He set about amassing evidence of evolution and trying to conceive of its causes. In 1838, at the age of 29, Darwin read an essay by the Charles Robert Darwin Futuyma Kirkpatrick Evolution, 4e Sinauer Associates Troutt Visual Services 12    CHAPTER 1 Nesomimus spp. Pinta Genovesa Galápagos Mockingbird N. parvulus Marchena Atlantic Santiago Ocean San Cristóbal Mockingbird N. melanotis Baltra Fernandina Santa San Equador Cruz Cristóbal Isabela Santa Fe Galápagos South Islands America Floréana Española (Equador) 20 km Pacific Ocean Floreana Mockingbird Española Mockingbird N. trifasciatus N. macdonaldi FIGURE 1.7 Four species of mockingbirds (Nesomimus) on different islands in the Galápagos archipelago were among the observations that led Darwin to suspect that different species evolve from a common ancestor. economist Thomas Malthus. Malthus argued that the rate of human population growth is greater than the rate of increase in the food supply, so that unchecked growth must lead to famine. This essay was the inspiration for Darwin’s great idea, one of the most important ideas in the history of thought: natural selection. Darwin wrote in his autobiography that “being well prepared to appreciate the struggle for existence which everywhere goes on from long-continued observa- tion of the habits of animals and plants, it at once struck me that under these circumstances favourable variations would tend to be preserved and unfavour- able ones to be destroyed.” In other words, of the many individuals that are born, not all survive; and if certain individuals with superior features survived and reproduced more successfully than individuals with inferior features, and if these differences were inherited, the average character of the species would be altered over the course of generations. Mindful of how controversial the subject would be, Darwin then spent 20 years developing his theory, amassing evidence, and pursuing other researches before publishing his ideas. In 1844 he wrote a private essay outlining his theory, and in 1856 he finally began a book he intended to call Natural Selection. He never completed it, for in June 1858 he received a manuscript from a young naturalist, Futuyma Kirkpatrick Evolution, 4e Sinauer Associates Evolution4e_01.07.ai Date 12-06-2016  Evolutionary Biology   13 (A) (B) FIGURE 1.8 Galápagos giant tortoises (Chelonoidis nigra) differ in shell shape among islands. Some subspecies, especially those that occupy humid highlands with low veg- etation, have a domed shell (A), whereas those in dry lowland habitats tend to have a “saddleback” shell (B) that enables the animal to extend its long neck to reach vegeta- tion higher above the ground. Alfred Russel Wallace (1823–1913). Wallace, who was collecting specimens in the Malay Archipelago, had independently conceived of natural selection. Darwin’s scientific colleagues presented extracts from his 1844 essay, along with Wal- lace’s manuscript, at a meeting of the major scientific society in London. Darwin immediately set about writing an “abstract” of the book he had intended. The 490-page result, titled On the Origin of Species by Means of Natural Selection, or The Preservation of Favoured Races in the Struggle for Life, was published on November 24, 1859; it instantly made Darwin, by now 50 years old, both a celebrity and a figure of controversy. For the rest of his life, Darwin continued to read and correspond on an immense range of subjects, to revise The Origin of Species (“on” was deleted from the title of later editions), to perform experiments of all sorts (especially on plants), and to publish many more articles and books, of which The Descent of Man is the most renowned. Darwin’s books reveal an irrepressibly inquisitive man, fascinated with all aspects of nature, creative in devising hypotheses and in bringing evidence to bear on them, and profoundly aware that every biological fact, no matter how seem- ingly trivial, must fit into a coherent, unified understanding of the world. Wallace Alfred Russel Wallace made significant further contributions to biology, especially about biogeography, the geographic distribution of species. He always gave credit to Darwin for the concept of natural selection, referring to it as “Mr. Darwin’s theory.” Darwin’s evolutionary theory The Origin of Species contains two major theories. The first is Darwin’s idea of descent with modification. It holds that all species, living and extinct, have descended, with- out interruption, from one or a few original forms of life (FIGURE 1.5B). Species that diverge from a common ancestor are at first very similar but accumulate differences over great spans of time, so that they may come to differ radically from one another. Darwin’s conception of the course of evolution is profoundly different from Lamarck’s, in which the concept of common ancestry plays almost no role. The second theory in The Origin of Species is natural selection, which Dar- win proposed is the chief cause of evolutionary change. He summarized it in the Futuyma Kirkpatrick Evolution, 4e Sinauer Associates Evolution4e_01.08.ai Date 12-06-2016 14    CHAPTER 1 following way: “If variations useful to any organic being ever occur, assuredly individuals thus characterized will have the best chance of being preserved in the struggle for life; and from the strong principle of inheritance, these will tend to produce offspring similarly characterized. This principle of preservation, or the survival of the fittest, I have called natural selection.” Unlike Lamarck’s transfor- mational theory, in which individual organisms change, Darwin’s is a variational theory of change, in which the frequency of a variant form (i.e., the proportion of individuals with that variant feature) increases within a population from genera- tion to generation (FIGURE 1.6B). Darwin proposed (as did Wallace) that fitter individuals differ only slightly from the norm of the population, but that a feature such as body size gradually evolves to become more and more different because new, slightly more extreme, advantageous variants continue to arise. Darwin’s theory of evolution includes five distinct components : 1. Evolution as such is the simple proposition that the characteristics of organisms change over time. Darwin was not the first to have this idea, but he so convincingly marshaled the evidence for evolution that most scientists soon accepted that it has indeed occurred. 2. Common descent: Differing radically from Lamarck, Darwin was the first to argue that species had diverged from common ancestors and that species could be portrayed as one great family tree representing actual ancestry (see Figure 1.5B). 3. Gradualism is Darwin’s proposition that the differences between even radically different organisms have evolved by small steps through intermediate forms, not by leaps (“saltations”). 4. Populational change is Darwin’s hypothesis that evolution occurs by changes in the proportions (frequencies) of different variant kinds of individuals within a population (see Figure 1.6B). This profoundly important, completely original idea contrasts with the sudden origin of new species by saltation and with Lamarckian transformation of individuals. For Darwin, the average was a statistical abstraction; there exist only varied individuals, and there are no fixed limits to the variation that a species may undergo [10, 18]. 5. Natural selection was Darwin’s brilliant hypothesis, independently conceived by Wallace, that accounts for adaptations, features that appear “designed” to fit organisms to their environment. Because it provided an entirely natural, mechanistic explanation for adaptive design that had previously been attributed to a divine intelligence, the concept of natural selection revolutionized not only biology, but Western thought as a whole. Darwin proposed that the various species that descend from a common ances- tor evolve different features because those features are adaptive under differ- ent “conditions of life”—different habitats or habits. Moreover, the pressure of competition favors the use of different foods or habitats by different species. He believed that no matter how extensively a species has diverged from its ancestor, new hereditary variations continue to arise, so that given enough time, there is no evident limit to the amount of divergence that can occur. Where, though, do these hereditary variations come from? This was the great gap in Darwin’s theory, and he never filled it. The problem was serious because, according to the prevailing belief in blending inheritance, variation should decrease, not increase. Because offspring are often intermediate between their parents in features such as color or size, it was widely believed that character- istics are inherited like fluids, such as paints of different colors. (This notion  Evolutionary Biology   15 persists today when people speak of having Italian or Indian “blood.”) Blending white and black paints produces gray, but mixing two gray paints yields more gray, not black or white. Darwin never knew that Gregor Mendel had solved the problem in a paper that was published in 1866, but not widely noticed until 1900. Mendel’s theory of particulate inheritance proposed that inheritance is based not on blending fluids, but on particles that pass unaltered from generation to generation—so that variation can persist. The concept of “mutation” in such particles (later called genes) was developed only after 1900 and was not clarified until considerably later. The Origin of Species is extraordinarily rich in insights and implications. Dar- win supported his hypotheses with an astonishingly broad variety of informa- tion, from variation in domesticated species to embryology to geographic pat- terns in the distribution of species. And he showed, or at least glimpsed, how research in every biological subject—taxonomy, paleontology, anatomy, embryol- ogy, biogeography, physiology, behavior, ecology—could be advanced and rein- terpreted in the light of evolution. Evolutionary biology after Darwin Although The Origin of Species raised enormous controversy, by the 1870s most scientists accepted the historical reality of evolution by descent, with modification, from common ancestors. This theory provided a new frame- work for exploring and interpreting the history and diversi- fication of life, a project that was especially promoted by the German zoologist Ernst Haeckel. Thus the late nineteenth and early twentieth centuries were a “golden age” of paleon- tology, comparative morphology, and comparative embryol- ogy, during which a great deal of information on evolution in the fossil record and on relationships among organisms was amassed. But the consensus did not extend to Dar- win’s theory of the cause of evolution, natural selection. For about 60 years after the publication of The Origin of Species, all but a few faithful Darwinians rejected natural selection, and numerous theories were proposed in its stead. These theories included neo-Lamarckian, orthogenetic, and muta- tionist theories. Neo-Lamarckism includes several theories based on the old idea of inheritance of modifications acquired during an organism’s lifetime. In a famous experiment, the German biologist August Weismann cut off the tails of mice for many generations and showed that this mutilation had no effect on the tail length of their descendants. Extensive subsequent research has provided no evidence that specific mutations can be induced by environmental conditions under which they would be advantageous. Theories of orthogenesis, or “straight-line evolution,” held that the variation that arises is directed toward fixed FIGURE 1.9 The extinct Irish elk (Megaloceros giganteus) had goals, so that a species evolves in a predetermined direction such enormous antlers that it was cited as an example of orthoge- by some kind of internal drive, without the aid of natural netic “momentum” that drove the species to evolve a maladap- selection. Some paleontologists held that such trends need tive feature that caused its extinction. Since the 1940s, evolution- not be adaptive and could even drive species toward extinc- ary biologists have rejected this idea. The huge antlers probably tion (FIGURE 1.9). None of the proponents of orthogenesis resulted from the animal’s overall large size and from natural ever proposed a mechanism for it. selection caused by competition among males for females. 16    CHAPTER 1 Mutationist theories were advanced by some geneticists who observed that discretely different new phenotypes can arise by a process of mutation. They sup- posed that such mutant forms constituted new species and thus believed that natural selection was not necessary to account for the origin of species. The last influential mutationist was Richard Goldschmidt (1940, ), an accomplished geneticist who nevertheless erroneously argued that the origin of new species and higher taxa is entirely different in kind from evolutionary change within species. New species or genera, he said, originate by sudden, drastic changes that reorganize the whole genome. Although most such reorganizations would be deleterious, a few “hopeful monsters” would be the progenitors of new forms of life. The evolutionary synthesis These anti-Darwinian ideas were refuted in the 1930s and 1940s by the geneti- cists, systematists, and paleontologists who reconciled Darwin’s theory with the facts of genetics [19, 28]. The consensus they forged is known as the evolutionary Ronald A. Fisher synthesis, or modern synthesis, and its chief principle, that adaptive evolution is caused by natural selection acting on particulate (Mendelian) genetic variation, is often referred to as neo-Darwinism.1 Ronald A. Fisher and John B. S. Haldane in England and Sewall Wright in the United States developed a mathematical theory of population genetics, which showed that mutation and natural selection together cause adaptive evolution: mutation is not an alternative to natural selection, but is rather its raw material. The study of genetic variation and change in natural popu- lations was pioneered in Russia by Sergei Chetverikov and continued by Theodo- sius Dobzhansky, who moved from Russia to the United States. In his influential book Genetics and the Origin of Species (1937, ), Dobzhansky conveyed the ideas of the population geneticists to other biologists, thus influencing their apprecia- tion of the genetic basis of evolution. Other major contributors to the synthesis included the zoologists Ernst Mayr, in Systematics and the Origin of Species (1942, ), and Bernhard Rensch, in Evolution Above the Species Level (1959, ); the botanist G. Ledyard Stebbins, in Variation and Evolution in Plants (1950, ); and the paleontologist George Gaylord Simpson, in Tempo and Mode in Evolution (1944, ) and its successor, The Major Features of Evolution (1953, ). These authors argued persuasively that mutation, gene flow or migration, natural selection, and genetic drift are the major causes of evolution within species (which Dobzhansky J. B. S. Haldane called microevolution)—and that continued over long periods of time, these same causes account for the origin of new species and for macroevolution: the evolution of the major alterations that distinguish higher taxa (genera, families, orders, and classes). The principal claims of the evolutionary synthesis are the foundations of modern evolutionary biology. Although some of these principles have been extended, clarified, or modified since the 1940s, most evolutionary biologists today accept them as substantially valid. They are summarized in BOX 1A. Evolutionary biology since the synthesis Since the evolutionary synthesis, a great deal of research has tested and elaborated its basic principles. These principles have largely been supported. Progress in evo- lutionary biology has modified some of these ideas and many extensions of these ideas, and it has spurred additional theory to account for new phenomena as they 1 “Neo-Darwinism” properly refers to Weismann’s strict version of Darwin’s theory of evolution by natural selection. Darwin had admitted a role for inheritance of acquired characteristics, but Weismann rejected this. Today, “neo-Darwinism” is often used to mean the theory articulated in the evolutionary synthesis. Sewall Wright  Evolutionary Biology   17 G. Ledyard Stebbins, George Gaylord Simpson, and Theodosius Dobzhansky were discovered. Since James Watson and Francis Crick established the structure of DNA in 1953, advances in genetics, molecular biology, and molecular and informa- tion technology have revolutionized the study of evolution. New molecular and computational technology has enabled new fields of evolutionary study to develop, among them molecular evolution (analysis of the processes and history of changes in genes). The leaders of the evolutionary syn- thesis had maintained that almost all features of organisms are adaptive, and evolved by natural selection. But this principle was challenged by the neutral theory of molecular evolution, developed by Motoo Kimura (1983, ), who argued that most of the evolution of DNA sequences occurs by chance (genetic drift) rather than by natural selection. Evolutionary developmental biology, growing out of comparative embryology and based partly on molecular genetics, is devoted to understanding how the evolution of developmental processes underlies the evolution of morphological features at all levels, from cells to whole organisms. Because the entire genome—the full DNA complement of an organism—can now be sequenced, molecular evolutionary studies have expanded into evolutionary genomics, which is concerned with variation and evolution in multiple genes or even entire genomes. Genomic data are enabling biologists to determine phylo- Motoo Kimura genetic relationships with ever-greater confidence; they are revealing the genetic bases of adaptive characteristics of species and how and when they were modified by natural selection, and they are revealing the history of populations and their distributions over the globe. The histories of species are written in their genes. The advances in these new fields are complemented by vigorous research, new discoveries, and new ideas about long-standing topics in evolutionary biology, such as the evolution of adaptations and of new species. Since the mid-1960s, evolutionary theory has expanded into areas such as ecology, animal behavior, and reproductive biology. Detailed theories that explain the evolution of particular kinds of characteristics such as life span, ecological distribution, and social behav- ior were pioneered by the evolutionary theoreticians William Hamilton and John Maynard Smith in England and George Williams in the United States. The study of macroevolution has been renewed by provocative interpretations of the fossil record and by new methods for studying phylogenetic relationships. Research in evolutionary biology is progressing more rapidly than ever before. Since Darwin’s time, research on evolution, and in biology more broadly, has transformed evolutionary biology. Were Darwin to reappear today, he would understand very few scientific papers about evolution. Modern evolutionary biology 18    CHAPTER 1 BOX 1A Fundamental Principles of Biological Evolution These are fundamental principles of evolution that ary change over time. Adaptations are traits that emerged from the modern synthesis. Much of the rest of have been shaped by natural selection. this book is devoted to explaining and building on them. 8. Natural selection can alter populations beyond the Some statements, marked by an asterisk (*), have to be original range of variation when changes in allele qualified to some degree, in light of later research. frequencies generate new combinations of genes. 1. An individual’s phenotype (its observed traits) is 9. Populations usually have considerable genetic distinct from its genotype (its DNA). Phenotypic differ- variation. Many populations evolve rapidly, to some ences among individuals are caused by both genetic degree, when environmental conditions change, differences and environmental effects. and do not have to wait for new favorable mutations. 2. Acquired characteristics are not inherited.* 10. The differences between species evolve by 3. Hereditary variations are based on particles—the rather small steps, and are often based on differ- genes.* This is true for traits with continuous variation ences at many genes that accumulated over many (e.g., body size) as well as those with discrete variation generations.* (e.g., eye color). 11. Species are groups of interbreeding or potentially 4. Genetic variation arises by random mutation. Muta- interbreeding individuals that do not exchange tions do not arise in response to need. Variation that genes with other such groups.* Species are not de- arises by mutation is amplified by recombination of fined simply by phenotypic differences. Rather, they alleles at different loci. represent separately evolving “gene pools.” 5. Evolution is a change of a population, not of an 12. Speciation (the origin of two species from a single individual. The elementary process of evolution is a ancestor species) usually occurs by the genetic change across generations in the frequencies of al- differentiation of geographically isolated popula- leles or genotypes, which can change the frequencies tions.* Species have genetic differences that pre- of phenotypes. vent interbreeding if they are no longer geographi- 6. Changes in allele frequencies may be random or cally separated. nonrandom. Natural selection results from differences 13. Higher taxa arise by the sequential accumulation among individuals in survival and reproduction, and of small differences, rather than by the sudden ap- causes nonrandom changes. Genetic drift causes pearance of drastically new types by mutation. random changes. 14. All organisms form a great Tree of Life (or phylog- 7. Natural selection can account for both slight and eny) that evolved by the branching of common an- great differences among species. Even a low intensity cestors into diverse lineages, chiefly by speciation. of natural selection can cause substantial evolution All forms of life descended from a single common ancestor that lived in the remote past. does not equal Darwinism, and any antievolutionary critiques of Darwin that do not take into account modern research are irrelevant to our understanding of evolution today. How Evolution Is Studied Evolutionary biology is a more historical science than most other biological dis- ciplines, for one of its goals is to determine what the history of life has been and what has caused those historical events. Occasionally we can document an evolutionary change as it occurs or piece together records to reconstruct a recent change, just as we do when studying  Evolutionary Biology   19 human history (see Chapter 3). Usually, however, we must infer evolutionary history and its causes by interpreting less direct evidence. Some historical events are inferred from fossils, the province of paleontology (see Chapters 17 and 19). Other evo- lutionary events are inferred from comparisons among living organisms or by studying their phylogenetic relationships, which provide a framework that enables us to draw conclusions about the historical evolution of their phenotypic characteris- tics and even their genes (see Chapters 2 and 16). The causes of evolution, such as genetic drift and natu- ral selection, are often studied by comparing data, such as patterns of variation in genes, with theoretical models (see Chapters 4–8). They are also studied by the methods of experimental evolution, in which laboratory populations of rap- idly reproducing organisms adapt to an environment (e.g., a stressful temperature) designed by an investigator (see Chap- ter 6). The adaptive reasons for certain characteristics (e.g., birdsong) may be inferred from experimental and other func- tional studies, from their “fit” to a theoretical design (e.g., the heart fits a “pump” design), or by comparing many popula- tions or species to see if the characteristic is correlated with a specific environmental factor or way of life (see Chapters 10–13). Certain patterns of variation in DNA sequences can tell us if natural selection has affected evolutionary changes in genes (see Chapters 5, 7, and 14). When we make inferences about history, or about past causes of change such as natural selection, we do not see the changes occurring, nor do we observe the causes in action. But throughout science, causes are not seen; rather, they are inferred. All of chem- istry, for example, concerns invisible atoms and orbitals that govern the association of atoms into molecules. These theoreti- cally postulated entities and their behavior have been confirmed Ernst Mayr, George C. Williams, John Maynard Smith because the theory that employs them makes predictions (hypotheses) that are matched by observed data. We know that DNA replicates semiconservatively not because anyone has ever seen DNA do that, but because the outcome of a famous experiment (and of later ones) matched the prediction made by the hypothesis. This hypothetico-deductive method, in which hypotheses are tested (and are rejected, modified, or provisionally accepted), has been a powerful tool through- out the sciences and is the basis of much evolutionary research. For example, would you predict that the DNA in mitochondria carries more mutations that are harmful to males than to females? There is no obvious biochemical reason to expect this, but evolutionary theory makes such a prediction. The mitochon- dria of both males and females are inherited from the mother; the mitochondria in males are not inherited via sperm and are thus at a “dead end.” If a muta- tion in mitochondrial DNA reduces the survival or reproduction of females, it is unlikely to be transmitted to subsequent generations, but the transmission of a mutation will not be affected if it is similarly harmful only to males, because males do not transmit the DNA anyway. So, male-deleterious mitochondrial mutations are expected to accumulate. This prediction, from the theory of natu- ral selection at the level of the gene, has been verified: mitochondrial variants commonly affect male, but not female, fertility in humans and other animals, and they cause variation in reproductive gene expression in male fruit flies [6, William D. Hamilton 20    CHAPTER 1 12]. This example illustrates how evolutionary hypotheses can be tested, and it also shows how they can predict and reveal aspects of biology we would not otherwise have expected. Philosophical Issues Thousands of pages have been written about the philosophical and social implica- tions of evolution. Darwin argued that every characteristic of a species can vary and can be altered radically, given enough time. Thus he rejected the emphasis on dis- tinct “types” that Western philosophy had inherited from Plato and Aristotle and put variation in its place. Darwin also helped replace a static conception of the world— one virtually identical to the Creator’s perfect creation—with a world of ceaseless change. It was Darwin who extended to living things, including the human species, the principle that change, not stasis, is the natural order. In contrast to traditional views that elevated the human species to a special position, distinct from other liv- ing things, Darwin began the trend to see humans as part of the natural world, a species of animal (though a very remarkable species, to be sure!) subject to the same processes as others, including natural selection. Darwin has been credited with making biology a science, for he proposed to replace supernatural explanations in biology with purely natural causes. His theory of random, purposeless variation acted on by blind, purposeless natural selection provided a revolutionary new kind of answer to almost all questions that begin with “Why?” Before Darwin, both philosophers and people in general answered questions such as “Why do plants have flowers?” or “Why are there apple trees?”—or diseases, or sexual reproduction—by imagining the possible purpose that God could have had in creating them. This kind of explanation was made completely superfluous by Darwin’s theory of natural selection. The adap- tations of organisms—long cited as the most conspicuous evidence of intelligent design in the universe—could be explained by purely mechanistic causes. For evolutionary biologists, the pink petals of a magnolia’s flower have a function (attracting pollinating insects) but not a purpose. The flower was not designed in order to propagate the species, much less to delight us with its beauty, but instead came into existence because magnolias with brightly colored flowers reproduced more prolifically than magnolias with duller flowers. The unsettling implication of this purely material explanation is that, except in the case of human behavior, we need not invoke, nor can we find any evidence for, any design, goal, or pur- pose anywhere in the natural world. All of modern science employs the way of thought that Darwin applied to biol- ogy. Geologists do not seek the purpose of earthquakes or plate tectonics, nor chemists the purpose of hydrogen bonds. The concept of purpose plays no part in scientific explanation.  Evolutionary Biology   21 Ethics, religion, and evolution In the world of science, the reality of evolution has not been in doubt for more than 100 years, but evolution remains an exceedingly controversial subject in the United States and a few other countries. The creationist movement opposes the teaching of evolution in public schools, or at least demands “equal time” for creationist beliefs. Such opposition arises from the fear that evolutionary science denies the existence of God, and consequently, that it denies any basis for rules of moral or ethical conduct. Science, including evolutionary biology, is silent on the existence of a super- natural being or a human soul, because these hypotheses cannot be tested. Many people, including some priests, ministers, rabbis, and evolutionary biologists, hold both religious beliefs and belief in evolution (see Chapter 22). But to explain phenomena in the natural world, science must assume that only natural causes operate, just as most people do in everyday affairs: we assume that there is a material cause when our car or computer or heart malfunctions. Supernatural explanations for observable phenomena often do conflict with naturalistic, scien- tific explanation. A literal reading of some passages in the Bible is incompatible with the principles of physics, geology, and other natural sciences. Our knowl- edge of the history and mechanisms of evolution is certainly incompatible with a literal reading of the creation stories in the Bible’s Book of Genesis—just as it is incompatible with hundreds of other creation myths people have devised. Wherever ethical and moral principles are to be found, it is probably not in science, and surely not in evolutionary biology. Opponents of evolution have charged that evolution by natural selection justifies the principle that “might makes right.” But evolutionary theory cannot provide any such precept for behavior. Like any other science, evolutionary biology describes how the world is, not how it should be. The supposition that what is “natural” is “good” is called by philosophers the naturalistic fallacy. Various animals have evolved behaviors that we give names such as coop- eration, monogamy, competition, infanticide, and the like. Whether or not these behaviors ought to be—and whether or not they are—moral, is not a scientific question. The natural world is amoral—the concepts of “moral” and “immoral” simply do not apply outside the realm of human behavior. Despite this, the concepts of natural selection and evolutionary progress were taken as a “law of nature” by which Marx justified class struggle, by which the Social Darwin- ists of the late eighteenth and early nineteenth centuries justified economic competition and imperialism, and by which the biologist Julian Huxley justi- fied humanitarianism [11, 21]. Most philosophers consider all these ideas to be indefensible instances of the naturalistic fallacy. Infanticide by lions and langur monkeys does not justify infanticide in humans; monogamy in penguins does not imply that humans should do the same. Evolution provides no basis for human ethics. Go to the Evolution Companion Website EVOLUTION4E.SINAUER.COM for data analysis and simulation exercises, quizzes, and more.