Portal de Periódicos da CAPES

History of Ecological Sciences, Part 52: Symbiosis Studies

2014; Ecological Society of America; Volume: 96; Issue: 1 Linguagem: Inglês

10.1890/0012-9623-96.1.80

2327-6096

Frank N. Egerton,

Animal Ecology and Behavior Studies

Symbiosis is a term that identifies persistent relationships between species, according to Surindar Paracer and Vernon Ahmadjian (2000:6). Their textbook discussed three kinds: commensalism, mutualism, and parasitism. Other kinds that some authors have identified, phoresis and inquilinism, they considered forms of commensalism. They also mentioned that some investigators have considered predation as a kind of symbiosis; they do not mention competition, which is often a persistent relationship within and between species. They also provided an outline: "Historical Landmarks of Symbiosis" (Paracer and Ahmadjian 2000:235–238), which skips from 1500 BC (Ebers papyrus) to AD 1200 (Albertus Magnus). Two small, not-quite textbooks entitled Symbiosis appeared in America in 1970, the much smaller by William Trager, Rockefeller University, and the much larger by Thomas Cheng, Lehigh University. Also in 1970, Clark Read, Rice University, published Parasitism and Symbiology: an Introductory Text. "Symbiosis is the most relevant and enduring biological theme in the history of our planet" (Stanley 2006:857). This is a modern echo of Pyotr (Peter) Kropotkin's claim of 1890 (see below). Although non-predatory species interactions are a major aspect of ecology (Henry 1966–1967, Margulis 1998, Paracer and Ahmadjian 2000), I am unaware of any general ecology textbook that reflects Stanley's claim for the importance of symbiosis in its organization. Some of Stanley's claim rests upon endosymbiosis—microorganisms living mutualistically within larger organisms—which Paul Buchner surveyed in detail (German 1953, revised in English, 1965)—and symbiogenesis of organelles within cells (Khakhina 1992); the latter is only indirectly within ecology's domain. Many types of symbiosis are inconspicuous and were overlooked until the later 1800s or during the 1900s, and some types still seem under-appreciated. Paul Buchner (1965:3–74) wrote a detailed history of studies on endosymbiosis of microorganisms with plants and animals, beginning in the mid-1800s. Jan Sapp wrote (1994) a useful history of symbiosis, with many more examples and details than are included in the present survey. He discussed symbiosis more briefly in his Genesis: The Evolution of Biology (2003:234–249). My organization of this essay differs from Sapp's, and I explore some topics he did not. For example, everyone knew that fruits contain seeds, and that seeds are the source of new plants. It was equally obvious that humans and various birds and mammals ate fruits. When did naturalists first comment on the fact that animals eating fruits are important disseminators of plant seeds? Sapp's history, which discussed symbiosis between plants and animals, included neither this aspect of it, nor even pollination. Whoever wishes to write a history of mutualism studies concerning seeds can begin with Henry Howe and Judith Smallwood's bibliographic guide, "Ecology of Seed Dispersal" (1982). A complexity is that some animal dispersal agents are also seed predators (Janzen 1971). Lee Dugatkin's The Altruism equation: seven scientists search for origins of goodness (2006) is comparatively narrow in scope, but scientists he discussed are important for symbiosis studies. The most fundamental symbiotic relationship is animals eating plant material and animal physiological wastes becoming fertilizer for plants. This was such a basic awareness in agrarian societies that it never received any special name or comment. Another symbiotic relationship so basic among agricultural societies that it received no special comment was human maintenance of domesticated animals. This could be seen as symbiotic only after the concept of symbiosis was defined. In antiquity, there were isolated examples of symbiosis described, plus an organizing concept, the balance of nature. Parasitism was the first symbiotic relationship recognized. The Egyptian Ebers medical papyrus (ca. 1550 BC) contained a prescription for killing intestinal round worms (quoted in Clendening 1942:4, Hoeppli 1959:5). The earliest contribution in antiquity to the balance of nature concept was by the Greek traveler–historian Herodotos (died ca. 425 BC), with his argument that Divine Providence had contrived to have predatory animals produce fewer offspring than their prey, thus preventing predators from eating all their food (Herodotos 1926–1938, volume 2, pages 135–137, book 3, section 108–109). Isolated examples of mutualism were reported in antiquity, beginning with Herodotos' report (1926–1938: volume 1, page 98, book 2, section 68) of Egyptian Plovers (Plovianus aegypticus or Hoplopterus armatus) picking leeches from inside the mouths of Nile crocodiles (Crocodylus niloticus), who, in "appreciation" for this service, never harmed the plovers. This also seemed to illustrate the balance of nature (Egerton 1973:326, 2001a:95–96, 2001b:151). Egyptian plover (Plovianus aegypticus) cleaning leeches from Nile crocodile (Crocodylus niloticus). Drawing by Kathryn H. Delisle. Sapp 1994:cover. In the sea between Cyrene and Egypt there is a fish called "louse," which dogs the dolphin; this fish gets extremely fat owing to the bountiful supplies of food available for its benefit when the dolphin is out hunting. Two species of remora inhabit the Mediterranean Sea (Thompson 1947:68). Historia Animalium also reported that the cuckoo Cuculus canorus lays eggs in the nests of other birds and disposes of the parasitized bird's own eggs (Aristotle 1965–1991: volume 2, 563b29–564a7). Historia Animalium (563b14–564a 6, 618a8–30) and Generatione Animalium (750a11–15) reported brood parasitism in the cuckoo (Cuculus canorus; Schultze-Hagen 2009), along with uncertainty about whether cuckoos can become transformed into hawks. They say that wild trees are not liable to diseases which destroy them, but that they get into poor condition, and that most obviously when they are smitten with hail when either they are about to bud or are just budding or are in bloom; also when either a cold or a hot wind comes at such seasons: but that from seasonable storms, even if they be violent, they take no hurt…. Cultivated kinds, however, they say, are subject to various diseases….being worm-eaten….also a "knot" (which some call a fungus, others a bark-blister)… …some plants are unable to sprout—either the seeds or the plants—in the ground, as the ixia [mistletoe, Loranthus europaeus], the stelis [Viscum album], and the hyphéar, stelis being the Euboean word, hyphéar the Arcadian, and ixia the word in general use. Some assert that all of them are a single natural entity, but because they grow on different plants they are also considered to be different: so the hyphéar occurs on the silver-fir and pine, and so too the stelis, whereas the ixia occurs on oak, terebinth, and a number of other trees. Roman authors on agriculture also discussed plant diseases, but without advancing beyond Theophrastos (Ainsworth 1981:14). Ainsworth (1981:41) and Paracer and Ahmadjian (2000:235) cite a description of (parasitic) mistletoe by Albertus Magnus (about 1200–1280) as a landmark, but without citation or details. Albert wrote De Vegetabilibus et plantis after 1250 (Egerton 1983, I:448). Albert did not know the botanical works by Theophrastos, which discussed mistletoe's growth on trees (Greene 1983, I:146 and Egerton's note 57 on pages 462–463). Albert's observations on oak galls are quoted in Egerton's history, part 9 (2003:88). Berries and other pericarps, are by nature allotted for aliment to animals, but with this condition, that while they eat the pulp they shall sow their seeds; for when they feed upon it they either disperse them at the same time, or, if they swallow them, they are returned with interest; for they always come out unhurt. Linnaeus then provided a variety of examples, including plants sprouting from manure applied as fertilizer, mistletoe being deposited by thrush droppings on tree limbs, crossbills dispersing seeds from fir cones, and swine turning up the earth while rooting for seeds. English physician Edward Jenner (1749–1823), remembered for his experiments leading to his establishment of smallpox vaccination (published in 1798), was also an early experimenter on bird behavior (Jenner 1788, Le Fanu 1951, Fisk 1959:86–96, Wilson 1973, Bircham 2007:113–116). He studied the parasitic cuckoos at the request of his former medical-surgical teacher, John Hunter. Jenner observed three species which cuckoos parasitized: titlark, water-wagtail, and hedge-sparrow. He found an egg which a cuckoo hatchling had expelled from the nest of the parasitized parent bird and restored it into the nest and noted its second expulsion. He commented that "The smallness of the Cuckoo egg in proportion to the size of the bird is a circumstance that hitherto, I believe, has escaped the notice of the ornithologist" (1788:227). A new aspect of symbiosis and balance of nature that developed in the mid and late 1700s was the study of pollination. It was obvious that bees and butterflies visited flowers to collect food, but the benefit to the plants was not obvious. Arthur Dobbs (1689–1765), an Irish Protestant member of the ruling class (governor of North Carolina, 1754–1765 [Chichester 1921, Snapp 1999, Calhoon 2004]), discovered the mutualism of pollination. His report appeared in the Philosophical Transactions of the Royal Society of London (1750). His attention might have been attracted by a swarm of busy bees, and he then consulted Réaumur's Mémoires pour servir à l'histoire des insectes (volume 5, 1740) for additional information. Or, perhaps he read Réaumur first and was then inspired to observe bees. At any rate, although highly praising Réaumur's work, when he read Réaumur contradicting Aristotle's claim that when a bee visits a particular kind of flower, it visits no other kind until it returns to the hive, Dobbs found that his observations supported Aristotle, and so he sent his observations to the Royal Society of London. Dobbs's observations were adequate to make his claim, and his article was quite clear, but it attracted no attention at the time (Grant 1949). Edward Jenner. Fisk 1959:book jacket. German botanist H. L. Hermann Müller (1829–1883), younger brother of zoologist Fritz Müller, wrote an encyclopedic Befruchtung der Blumen (1873), updated and translated into English (1883), with posthumous preface by Darwin. Müller's book has a good historical introduction (1883:1–29, 1977), though he was unaware of Dobbs's 1750 article. It began therefore, with Christian K. Sprengel's Das entdeckte Geheimniss der Natur im Bau und in der Befruchtung der Blumen (1793), an encyclopedic survey (Egerton 2008:170–171). Sprengel (1750–1816) was rector of a Lutheran school and an amateur botanist (King 1975). He concluded that some flowers cannot be fertilized without the assistance of insects, and that the function of flowers and nectar is to entice them into performing this task. He explained his initial discoveries on page one of his book, which Fredrick Bodenheimer translated into English in his history of biology (1958:333–340). Sprengel then proceeded to study flower morphology to learn how it guides insects to ensure fertilization. He observed that while gathering nectar, insects carry pollen from the anthers of one plant to the stigma of another, but he failed to wonder why cross-fertilization seemed necessary. Müller thought that this omission was why Sprengel's monograph attracted little attention from botanists. Subsequently, three botanists published studies indicating that cross-fertilization was necessary for producing healthy plants (Knight 1799, Herbert 1837, Gärtner 1844–49). However, it took the new context provided by Darwin's Origin of Species (1859) to attract general interest in pollination studies. Another new aspect of symbiosis and balance of nature during the later 1700s was the identification, first, of different kinds of gases, and second, the discovery that animals need one gas (oxygen), which plants emit, and plants need another gas (carbon dioxide), which animals emit. This discovery emerged from the chemical–plant–animal investigations that Joseph Priestley, Jan Ingen-Housz, and Jean Senebier conducted during the 1770s–1780s (Egerton 2008a:164–169). Studies on plant diseases and on animal diseases and parasites made substantial progress during the 1700s, but without breakthrough establishment of a germ theory of disease (Egerton 2008b, c). The blood-sucking habit of vampire bats was known to the Mayan and other Central and South American Indians before the arrival of Europeans in America, and the entourage of Hernando Cortés (1485–1547), conqueror of Mexico in the early 1500s, received reports of about it (Villa and Canela 1988). In March, 1800, Alexander von Humboldt (1769–1859) encountered them on the plains (llanos) of Venezuela, attacking his horses (Botting 1973:95), and Charles Darwin (Darwin 1838:25) collected a new species attacking his horses in Brazil in April, 1832. Foraging conditions and foraging modes may have favored parasitism in some groups. Many brood parasites are nomadic, following food resources. Cuckoos wander around assessing local foraging conditions, becoming numerous during local population outbreaks of caterpillars. Honeyguides also wander in search of beehives, and cowbirds presumably used to follow roaming herds of Bison. These three groups of brood parasites, therefore, are nomadic, and becoming sedentary for the time required to set up a territory, construct a nest, incubate eggs, and raise young would be problematic. Pollination of Salvia pratensis. Sprengel (1793). From Bodenheimer 1958:338. Sprengel's drawing of bee pollination of Nigella arvensis is reproduced in Egerton 2008a:170. No need to speculate about cowbirds and bison. The Lewis and Clark Expedition (1804–06) into America's northwest (Egerton 2009:440–448) in their journals called cowbirds "buffalo-pecker," which ornithologist-editor Elliot Coues (1893, 1965:1081) explained came from a habit of these birds of picking ticks off the backs of bison. Alexander Wilson (1766–1813) was not the discoverer of parasitism in cowbirds Molothrus ater, but he was a careful observer of them and published the first detailed account of them in volume 2 (1810) of his American Ornithology, showing a parasitized Maryland Yellowthroat parent feeding a young cowbird. Having grown up in Scotland (Egerton 2009:454–459), he was previously aware of brood parasitism in European cuckoos. American naturalist Henry Thoreau (1817–62) had an ecological outlook on nature and sought connections between species (Egerton 2011a). His insightful essay, "The Succession of Forest Trees" (1860, 1980), discussed squirrels planting oak trees by burying more acorns than they ever dug up, and wood mice doing the same with chestnuts. He also acknowledged that Linnaeus had said that "while the swine is rooting for acorns he is planting acorns" (1980:90). Thoreau was citing Linnaeus from memory and did not quite convey details correctly, but did capture the explanation's essence. Cowbirds Molothrus ater: 1. Male, 2. Female, 3. Young being fed by parasitized parent, 4. Maryland Yellowthroat. Wilson 1808–1814, II, plate 18. Darwin's theory of evolution by natural selection (1859) emphasized struggle for existence and is logically incompatible with Linnaeus's economy of nature (Limoges 1970:151, Egerton 1973:341). However, that incompatibility was overlooked by Darwin and his contemporary followers. Darwin himself noted what we call symbiotic relationships, such as dependency of mistletoe upon insects for pollination and birds for disseminating its seeds (Darwin 1859:3), and reciprocal dependence of flowers on pollinating insects and of insects on flowers making pollen and nectar (Darwin 1859:92–93). "Darwin influenced pollination ecology more deeply than anybody else during the nineteenth century" (Müller 1883:4–11, Faegri and van der Pijl 1971:3). His hypothetical food chain—clover, bees, mice, cats (Darwin 1859:73–74)—illustrates symbiotic relationships (clover–bees, bees–mice), though some links in the chain have limited validity (McAtee 1947, Egerton 2007:52–53). In On the Origin of Species (Darwin 1859:3361–363), Darwin discussed the dissemination of seeds at the biogeographical scale and pointed out that some fruit-eating birds can fly 35 miles an hour, and even faster when caught by a gale, and so they can often defecate viable seeds far from where they ate their food. Darwin's focus concerning seed dissemination was not symbiosis, but he took that fact for granted. Darwin's studies on orchid fertilization by insects (1860–1861–1862) was a detailed study of symbiotic relationships within an evolutionary context. My previous illustrated discussion of this subject is online (Egerton 2011b:359–363). This difficulty, though appearing insuperable, is lessened, or, as I believe, disappears, when it is remembered that selection may be applied to the family, as well as to the individual, and may thus gain the desired end. This was a one-sentence response which could easily be lost from memory as one continued to read his various complex resolutions to other questions. The significance of Darwin's work in general and the Origin in particular for symbiosis studies lay less in the particular examples that he discussed than in the new paradigm that he provided, with which it became possible to view symbiotic relationships as having evolved over time. Early participants in Darwin's revolution were fellow Englishmen Henry Walter Bates (1825–1892) and Alfred Russel Wallace (1823–1913), who left England in 1848 to explore Amazonia. Bates stayed until 1859, seven years longer than Wallace (Bates 1863, McKinney 1970, 1976, Dickenson 2004, Egerton 2012a:42–49, Drouin 2014:151–157). He returned to England just before Darwin published the Origin, and became an immediate convert to Darwin's theory when he read that book. When Bates in 1861 read to the Linnean Society of London his paper on Leptalis butterflies mimicking color patterns of Heliconiidae butterflies (published 1862), he was among the earliest to provide new evidence for Darwin's theory of evolution by natural selection (Blaisdale 1992:63–141). Batesian mimicry occurs when a palatable species evolves to resemble an unpalatable species. Remarkably, Wallace (1865:18–22) found a parallel case of mimicry among the Papilionidae of Malaya (Blaisdale 1992:144–156), which he reported to the Linnean Society in 1864 (published 1865). On the basis of his and Bates's studies, Wallace announced laws of mimicry, which German zoologist Fritz Müller (1822–1897) challenged on the basis of his own studies (Blaisdale 1992:186–197). Müller, older brother of botanist Hermann Müller, had received a Ph.D. degree at Berlin under Johannes Müller in 1844 (McKinney 1974). He permanently immigrated to southern Brazil, where he wrote Für Darwin (1864, English 1869), which earned him Darwin's lifelong friendship. Müllerian mimicry (1879) differed from Batesian mimicry in that both species of butterflies were about equally distasteful to predators, and by coming to resemble each other, predators learned more quickly of their distastefulness. Several species of Euglossini orchid bees exhibit Müllerian mimicry (Dressler 1982:375). In contrast to Bates's ready acceptance of Darwin's theory of evolution, Yale University geology professor James Dana (1813–1995), who had readily accepted Darwin's theory of coral reefs in the 1840s, and later had only minor changes to suggest (Dana 1885), was a tardy convert. Dana had corresponded with Darwin—and had received an autographed copy of the Origin—and was friends with evolutionist Asa Gray. However, Dana struggled until ca. 1874 before accepting Darwin's theory of evolution by natural selection (Sanford 1965, Stanton 1971:553). Dana's version of evolution was a mixture of Darwinism and Lamarckism. All scientific revolutions have immediate defenders and slow converts. Intraspecific cooperation is sometimes considered an aspect of symbiosis, though not by Paracer and Ahmadjian (2000). That social species—wolves, lions, many primates, elephants, many hoofed mammals, meerkats, aquatic mammals, some fish, ants, honey bees, termites—engage in cooperation was common knowledge since antiquity. Alfred Espinas (1844–1922) was a French philosopher, author of Des Sociétés Animales (1878, English 1935), who wrote his doctoral dissertation in Paris (Mitman 1992:65–66, Brooks 1998:97–133, Egerton 2014a:59–60). His understanding of evolution came from Herbert Spencer. Espinas's book was the first comprehensive survey of animal mutualism within species: coral, social insects, fish, reptiles, birds, mammals, and humans. Darwin's emphasis upon struggle for existence was carried to an extreme by his "bulldog," Thomas H. Huxley (1888), which prompted a Russian prince, naturalist, geographer, and exiled anarchist, Pyotr (later, Peter) A. Kropotkin (1842–1921), to publish "Mutual Aid among Animals" (1890), and articles on mutual aid among humans, all of which he collected into a much-read book, Mutual Aid (1902); both versions drew upon his own Siberian observations (Naumov 1973, Miller 1976, Mitman 1992:66–67, Sapp 1994:20–23, Dugatkin 2006:12–36, 2011, Borrello 2010:30–38, Hale 2014:227–235). He acknowledged that his awareness of this issue came from a lecture by St. Petersburg University Professor of Ichthyology Karl Fiodorvic Kessler, "Mutual Aid among Animals" (1880), in which Kessler said: "Mutual aid is as much a law of nature as mutual struggle; but for the progressive evolution of the species the former is far more important than the latter" (quoted in Kropotkin 1899:498; Miller 1976:173, Todes 1987:545–546). Kropotkin's autobiography did not mention Espinas. Kropotkin grew up in luxury in, and sometimes near, Moscow, and he developed an early fondness for nature. His very conservative father unknowingly hired two young radicals as tutors of his three children, one a student at Moscow, the other a Frenchman, who taught about the French Revolution along with the French language (Kropotkin 1899:15–18). Pyotr's hero became Alexander von Humboldt, whose Cosmos he read, and he wanted to explore Siberia just as Humboldt had explored tropical America. At age 15 he was sent to the emperor's Corps of Pages, in St. Petersburg, for education as a government administrator or army officer. Pyotr found it very boring, and at the end of five years he did not ask for assignment to any of the positions most coveted by other students. Rather, he wanted to go to the Amur River Valley in Siberia (Kropotkin 1899:154–157). Nature in Siberia met his expectations. He took five expeditions to explore and sometimes to map regions that had never been mapped. However, he felt that government was a burden to the people rather than an aid to them. After five years in Siberia, Kropotkin returned in 1867 to St. Petersburg and spent the next five years partly at its university, studying mathematics, science, and especially geography, and also much time at the Russian Geographical Society (Kropotkin 1899:224–225, Miller 1976:72–73, Dugatkin 2011:18–19). Yet he was distracted by anarchist politics and joined a group that gave books and assistance to the working class. These activities landed him in prison, from which he escaped after a year, in 1876, and he went to England, where he could speak his mind. A trip to France, however, also landed him in prison, but influential allies in France and England applied pressure to the French government, causing his release back to England. Kropotkin saw the same impulse for cooperation in humans that he saw in nature, and he thought that if social species of animals live without government, so could humanity. One of America's two leading entomologists in the early 1900s was Milwaukeean William Morton Wheeler (1865–1937), who mainly studied ants, which eventually led to a special interest in social insect species (Evans and Evans 1970, Mallis 1971:362–368, Shor 1976, Burgess 1996:110–112). (The other leading entomologist was John H. Comstock, 1849–1931, [Egerton 2013a:55–58]) Wheeler's broader interest was encouraged by an invitation to lecture before the Lowell Institute in Boston in 1921. Those six lectures then became chapters in his book, Social Life among the Insects (1923), on beetles, wasps, bees, ants, parasitic ants and ant guests, and termites. The fifth chapter, on parasitic ants and ant guests, shows how intraspecific cooperation can lead to interspecific relationships. Wheeler argued that an ant colony can be considered as an organism (1911) or superorganism (1928) (Wheeler 1911, 1928; Evans and Evans 1970:255–256, 263–266, Wilson 1971:317–318, Borrello 2010:28–29). The revival of the latter term occurs in the title of Bert Hölldobler and Edward O. Wilson's The Superorganism: the Beauty, Elegance, and Strangeness of Insect Societies (2009). Indianian W. Clyde Allee (1885–1955), a Quaker, attended a Quaker college, Earlham (B.S., 1908), and was a graduate student in zoology at the University of Chicago under Victor Shelford (M.S, 1910, Ph.D., 1912). After having several positions elsewhere, he returned to the University of Chicago in 1921 (Engel 1983:172–183, Kimler 1990, Mitman 1988, 1992, 1999, Sapp 1994:137–139, Burgess 1996:11, Sterling 1997a, Dugatkin 2006:37–60). Allee acknowledged that his pacifism influenced his choice of research topics, but claimed his research was nevertheless objective. He studied animal aggregations, a social formation intermediate between individuals and communities. He published books on it—Animal Aggregations (1931), Animal Life and Social Growth (1932), The Social Life of Animals (1938)–and he interested students in conducting research on it. His ally at Chicago was zoologist Alfred E. Emerson (1896–1976) from Ithaca, New York, who earned his degrees at Cornell University under Comstock (B.S., 1918, M.S., 1920, Ph.D., 1925). (Park 1967, Wilson and Michener 1982, Burgess 1996:39–40). He became the leading world authority on termites, and he wrote the chapters on insect societies in their Principles of Animal Ecology (Allee et al. 1949: chapters 24, 31–35). Pyotr A. Kropotkin, age 22. Kroptkin 1899:facing 210. William Morton Wheeler collecting ants in a New South Wales national park, Australia, 1931. Archives of Museum of Comparative Zoology, Harvard University. The modern theory of genetic theory of altruism, selfishness, and spite was launched…by William D. Hamilton in a series of important articles (1964, 1970, 1971a, b, 1972). Hamilton's pivotal concept is inclusive fitness: the sum of an individual's own fitness plus the sum of all the effects it causes to the related parts of the fitnesses of all its relatives. He made two trips to the Congo Valley to study HIV virus, contracted malaria on the second trip and died shortly after returning home, age 63. Harvard University Professor Edward O. Wilson (b. 1929) wrote that Hamilton's "seminal theory of kin selection" (Wilson 1994:315) was the most important "element" in sociobiological theory, but that he could not accept it upon first reading. Wilson is not only a world authority on ants, as Wheeler had been, but also a leading ecologist and evolutionist. His The Insect Societies (1971) discussed in most detail intraspecific cooperation; chapter 19 is on symbiosis between ant species, and chapter 20 is on symbiosis between ant species and other arthropod species. Wilson broadened the scope of his investigations in Sociobiology: the New Synthesis (1975), which attracted about the same degree of controversy as Darwin's Origin had (Ruse 1979, Segerstrâle 2000). Subsequently, intraspecific cooperation was investigated by sociobiologists (Wilson 1975:120–129, 1994:315–327). University of Louisville Professor Lee Dugatkin (b. 1962) provided a recent synthesis, Cooperation among Animals: An Evolutionary Perspective (1997), limited to intraspecific relationships, but in his Principles of Animal Behavior (Dugatkin 2009 [edition 2]:326–332) he also discussed mutualism between species. Stanford University Professor Joan Roughgarden (b. 1946) challenged both Richard Dawkins, The Selfish Gene (1976) and aspects of sociobiology in The Genial Gene: Deconstructing Darwinian Selfishness (2009). A controversy between defenders of "selfish" vs. "genial" genes may be long lasting. Diagram of the factoral complex influencing the population of typical termites of the family Rhinotermitidae. Arrows indicate direction of effects. Allee et al. 1949:722. One aspect of intraspecific cooperation that has received recent attention is assistance in raising young offspring ("cooperative breeding"), seen in some species of both birds (Woolfenden and Fitzpatrick 1984, 1996:16–17, Skutch 1999, Dugatkin 2006:120–121) and mammals, including wolves (Allen 1979:260–264). However, the human ability to cooperate on large scales, as Frans de Waal (2014) and Gary Stix (2014) argue, was a huge asset in human rise to world dominance. Since predation has been commonly observed before the Greeks and ever since, it is impracticable to survey such studies. What seems practicable is to mention studies that provide significant new insights. Should an insect eating a plant leaf be called a predator? That seems preferable (to me) to calling them parasites. Ehrlich and Raven might disagree. The idea that plant secondary compounds evolved as defenses against insect herbivores had been suggested by Fraenkel (1956, 1959); and much of Ehrlich and Raven's paper is a comprehensive survey of patterns of host plant use by different taxa of butterflies. To explain these patterns, they define the process of coevolution…. Ehrlich and Raven referred to these butterflies as "phytophagous or parasitic organisms" (1964:600). But if a caterpillar eating a