Meaning of YEAR IN REVIEW 2001: LIFE-SCIENCES in English

Botany The potential dangers of genetically modified (GM) plants continued to be debated in 2000. The issue grew increasingly heated in both Western Europe and the U.S. as concerns were expressed about the effects of the plants on the environment and human health. Policy makers in Europe set new restrictions on how far away from conventional crops GM crops undergoing field trials had to be grown to prevent transfer of GM plant pollen, but these limits were later shown to be highly suspect as to their effectiveness. Results of the first large-scale study of the flow of genetic material from GM oilseed rape to its wild relatives suggested that hybridization between crops and weeds is rare but that it does occur. Alarm was also raised over the accidental planting of GM oilseed rape on several farms in Europe. That the problem of inadvertent mixing could be widespread was suggested by results of a random sampling conducted by a company that screened for GM material. Genetic ID of Fairfield, Iowa, found that more than half the samples of conventional seed taken from American distributors contained some GM seeds. Another controversy continued to brew over so-called GM terminator seeds. These seeds can give rise to only one generation of plants; the next-generation seeds are sterile. Poor farmers in the less-developed world saw this technology as a serious economic threat because they relied on saving some seeds from their crop for the next year's planting. In August the U.S. Department of Agriculture (USDA) announced that it would sanction the terminator technology, albeit with conditions to guard against environmental damage-for example, from cross-pollination with conventional crops, which might then become sterile. (The USDA was a joint patent holder of terminator technology, but it also regulated the engineered seeds to ensure that they were safe enough to be field-tested and sold commercially.) Biotechnology protesters vehemently opposed the decision. Despite significant biological and ethical concerns, the potential benefits of GM crops remained tantalizing. During the year a gene that helps determine the size of fruit in tomato plants was identified by Anne Frary, Steven Tanksley, and colleagues of Cornell University, Ithaca, N.Y.-the first time that a gene for a quantitative trait such as height or weight had been found in plants. Because related genes exist in many other plant species, the discovery could lead to the genetic engineering of giant fruit, vegetables, or grain and the development of small wild plants into new, larger crops. GM crops also had considerable potential to be tailored into products having therapeutic and health benefits. In September Charles Arntzen of Cornell University reported that his team had genetically engineered a vaccine into tomatoes and bananas that could wipe out hepatitis B and thus potentially save hundreds of thousands of lives each year. The edible vaccine awaited a license from the USDA to allow the plants to be grown commercially. (See Agriculture: Special Report.) The excitement surrounding GM research had a tendency to overshadow significant conventional plant-breeding work. A team at the John Innes Centre, Norwich, Eng., announced in May at an Institute of Food Research seminar in London that it had bred a "superbroccoli" by crossing ordinary broccoli with a wild relative that contains 10 times as much sulforaphane, a compound that helps neutralize cancer-causing substances in the human digestive tract. USDA researcher David Garvin and colleagues also pinpointed the gene in a strain of barley that allows it to tolerate high levels of aluminum in the soil. Aluminum toxicity blights half the world's arable land, and the discovery opened up the possibility of breeding aluminum tolerance into other crops and thus exploiting huge barren tracts. Fascinating insights were gained into the ways that plants fight off insect attacks. Whereas plants suffering damage by insects were known to release airborne chemicals to attract natural predators of the pests, lima bean plants under attack by mites also switch on the defenses of neighbouring plants to attract predators. A team led by Gen-ichiro Arimura of the Bio-oriented Technology Research Advancement Institution in Tokyo found that three volatile terpenoids released by the besieged plants turn on the defense genes of their neighbours. These chemicals potentially could be used in new "natural" forms of crop protection. Plants also were found to use astonishing defenses against insect eggs laid on the plants. A new class of compounds called bruchins was discovered in pea weevils during their egg-laying activity on pea plants. The chemicals switch on a gene in the plants that causes them to surround the weevil's eggs with small tumourlike growths, which impede the larvae after they hatch. For the first time, the explosive fertilization of a flower was observed. After a pollen grain lands on a flower's stigma, it germinates, sending a growing pollen tube down the style. When the pollen tube enters the flower's embryo sac, it thrusts between the two sterile, synergid cells located on either side of the egg, ruptures its tip, and releases its gametes. Tetsuya Higashiyama of the University of Tokyo and colleagues recorded the pollen tube exploding, discharging its contents at a flow rate some 50 times higher than the cytoplasmic flow observed in the tube prior to discharge, and instantly pulverizing one of the synergid cells. Assumptions about how trees respond to global warming and elevated atmospheric carbon dioxide were proving more complex than first thought. A study of tree growth in Alaska revealed that higher mean temperatures in the past century had caused drought and stress. This finding upset calculations that the northern forests would absorb some of the additional carbon dioxide being blamed for the rise in world temperatures. The British government's Hadley Centre for Climate Prediction and Research near London warned that global warming could wipe out a third of the Amazon rain forest by the end of the 21st century owing to rising temperatures and drought. Efforts to conserve plant species from extinction relied increasingly on storing seeds in seed banks, but disturbing evidence uncovered some alarming shortcomings with these banks. According to Stefano Padulosi of the International Plant Genetic Resources Institute in Rome, of 5,300 species of food plants collected worldwide, more than half had only a single sample left in a seed bank, even though each species may have hundreds or thousands of varieties. Many collections were being destroyed by seed banks short of money, especially in less-developed countries. Many of the stored seeds were also losing their viability. Either the seeds needed to be sown every few years and fresh seed collected, or they had to be stored in deep-freeze facilities. Most seed banks, however, did not have freezers. Paul Simons Molecular Biology Among the landmarks of human achievement, a major milestone was reported in 2000-the completion of a rough draft of the sequence of the human nuclear genome. This tome consists of more than three billion characters, arranged as linear sets of carefully ordered nucleic acid bases. The accomplishment was of profound significance and promised revolutionary advances not only in biology and medicine but also in the way humans perceive themselves. (See Special Report.) Paleontology Studies in paleontology during 2000 offered intriguing new information on topics ranging from the origins of fish and feathers to long-term evolutionary patterns in marine communities. Until that time, little was known about the origin of vertebrates. While the Cambrian Period marked the beginning of an explosive evolutionary radiation among the major groups of invertebrates with hard parts, fish were absent from this first phase of rapid diversification of multicelled animals. Recently described finds from the Early Cambrian Chengjiang beds of China, however, included delicate small fossils that revealed vertebrate-like skulls, gills, and muscles. These specimens pushed the known origin of vertebrates back by as much as 50 million years; previously, the oldest known fish were from the Late Cambrian. Bony fish were the most diverse group (greatest number of species) of vertebrates, yet few fossils have been found that offer details of their origin and subsequent split into the ray-finned and lobe-finned clades. (A clade is a single lineage composed of a common ancestor and all of its descendants.) A recent paper published by a paleontologist from the Chinese Academy of Sciences' Institute of Vertebrate Paleontology and Paleoanthropology in Beijing, however, extended the fossil record of bony fishes back to the boundary of the Silurian and Devonian periods, about 408 million years ago. Unlike previous early bony-fish fossils, the Chinese specimen included a mixture of lobe-finned and ray-finned features and thus could provide insight into the origin of bony fish from more primitive types of fish. A second study on early bony fish described the most primitive braincase ever found of a ray-finned fish. This 400 million-year-old specimen from southeastern Australia exhibited primitive features previously unknown from any bony-fish fossils, including an opening for a cartilaginous eyestalk. A controversial paper published in June again raised the issue of feathered reptiles and the origin of birds. After having been housed in a Russian research institute for decades, a 220 million-year-old fossil of a reptile named Longisquama insignis was reevaluated by a group of Russian and American scientists and determined to have had featherlike appendages. The scientists further suggested that the mouse-sized creature could have been an ancestor of modern birds. Because Longisquama was not a dinosaur and may not even have been an archosaur (a larger group that includes some primitive reptiles as well as dinosaurs, crocodiles, and pterosaurs), this suggestion conflicted with the prevailing idea supported by most paleontologists that birds evolved from theropods (carnivorous dinosaurs, including Tyrannosaurus). Critics of the study claimed that the structures described may not have been feathers at all but could instead have been indicative of large membranous scales. They also argued that even if the structures were feathers or featherlike, other birdlike features were not present in this primitive reptile. A complete analysis that included all of the important derived features of birds continued to place them with the theropod dinosaurs. A third specimen of the much-debated feathered theropod dinosaur, Caudipteryx, was described during the year by a scientist at the Institute of Vertebrate Paleontology and Paleoanthropology. Although the specimen lacked a head, the report indicated that it had well-preserved feather impressions and that the skeleton was much better preserved than those of the two earlier specimens described in 1998. The study claimed that although the specimen exhibited some new bird features that were generally not found in theropods, such as an appendage on the foot for perching, it also had 16 dinosaur-like characteristics previously unknown in Caudipteryx. Though many seemed convinced that these findings added new strength to the view that dinosaurs and birds are related, others questioned whether this animal had true avian feathers. A study of 12 articulated ornithomimid dinosaur skeletons discovered in 1997 in the Cretaceous Ulansuhai Formation in China revealed some startling new information about the diet of ornithomimids. Although ornithomimids were toothless, they clearly were theropod dinosaurs; consequently, it was long assumed that they were probably toothless carnivores, feeding on small prey much like modern carnivorous birds. These new skeletons, however, had preserved masses of gastroliths inside the rib cage of each animal. Gastroliths are commonly known as "stomach stones," and they have also been found in the rib cages of many of the large sauropod dinosaurs, such as Apatosaurus. The presence of gastroliths suggested that ornithomimids, like the sauropods, were herbivorous rather than carnivorous. The gastroliths function as a grinding mechanism in the stomach to aid in the digestion of coarse plant material. Many modern herbivorous birds use fine-grained gravel or grit in a similar fashion to grind up plant material in the stomach. Investigators described an oviraptorosaur from Mongolia with a pygostyle, which suggested that this small theropod dinosaur may have had a tail fan of elongate feathers. The pygostyle, comprising several fused vertebrae at the end of the tail, is typically found only in birds. Because other features, however, place oviraptorosaurs at some distance from the origin of birds, the investigators suggested that this structure originated independently in the two groups. A recent study by a researcher at the National Geological Museum of China and others described Jeholodens jenkinsi, the most complete skeleton of a triconodont ever found. Members of the order Triconodonta were among the earliest (Late Triassic Epoch, 230 million to 208 million years ago) mammals known from the fossil record. They represent a clade much more primitive than even the modern egg-laying monotremes. Jeholodens exhibited predominantly primitive characteristics, but the structure of its shoulder was somewhat similar to that of more advanced mammal groups. This feature of Jeholodens apparently evolved independently of the advanced shoulder of modern mammals. A primitive, limbed fossil snake from the Middle East was reported during the year in the journal Science. This 95 million-year-old fossil found in carbonate deposits near Jerusalem preserved portions of the hind limb, including the tibia, fibula, metatarsals, and phalanges. This species, Haasiophis terrasanctus, appears to be evolutionarily near the time when snakes evolved from their limbed predecessors. Loss of limbs is an event that may have occurred more than once during the evolution of snakes in the Late Cretaceous. The extinctions of large terrestrial mammals and birds during the Quaternary Period (1.6 million years ago to the present) have long been a subject of debate among paleontologists. Contrasting theories blame the extinction on either dramatic climatic change or hunting by primitive human groups. A new study of the fossil record of a large flightless bird from Australia provided new evidence that climate was not a factor in these extinctions. The disappearance of this bird occurred approximately 50,000 years ago, a time when humans first arrived in Australia but not a time of major climate change. Owing to the poor nature of the hominid fossil record, little has been known about the origin of bipedalism in hominids. A report published during the year on specimens of Australopithecus anamensis and A. afarensis indicated that those primitive hominids retained the specialized wrist structure and function associated with knuckle-walking primates. Because Australopithecus was clearly a hominid, this suggested that bipedalism evolved from knuckle-walking ancestors. The fossil record often shows that when a new superior group of organisms arises, older, more primitive groups cannot compete and are quickly driven to extinction. Several paleontologists, however, reported that evolutionary patterns in bryozoans suggest that survival of the fittest does not necessarily require extinction of the less fit. They contended that the older cyclostome bryozoans coexisted with the newer cheilostomes for tens of millions of years during the Mesozoic Era until the mass extinction at the end of the Cretaceous Period 66.4 million years ago dramatically reduced the diversity of both groups. It was only then that the more advanced cheilostomes were able to significantly surpass the diversity level of the cyclostomes, which did not rebound from the extinction. A recent analysis of long-term evolutionary patterns claimed that major changes in marine communities since the beginning of the Phanerozoic Eon about 540 million years ago correlated with increased diversity in terrestrial communities. This was one of the first studies to link diversity trends in terrestrial and marine organisms. William R. Hammer Zoology Research on animals in 2000 ranged from tiny hummingbirds to the giant extinct moas, delved into the evolutionary responses of prey to predators, and focused on dolphins to gain insight into the development of language. Issues in conservation biology continued to dominate concerns about wildlife on a global scale. Dolphins were considered to be among the most intelligent of nonhuman animals because of their large brains, their advanced social behaviour, and their ability-observed in captivity-to communicate with each other by whistling. A study by Vincent M. Janik of the University of St. Andrews, Scot., provided evidence that dolphin whistles are used for social communication between individuals in the wild. Captive dolphins previously had been documented to repeat underwater whistles immediately upon first hearing them and to develop individualized signature whistles with distinctive frequency patterns. To test the effectiveness of whistle communication in wild dolphins while avoiding observer effects, Janik analyzed recordings of hydrophones that had been placed in an area inhabited by groups of bottle-nosed dolphins (Tursiops truncatus) in the Kessock Channel of Moray Firth, Scotland. More than 1,700 whistles were recorded in instances when an average of 10 dolphins were in the vicinity. Of the total number of recorded whistles, Janik was able to pinpoint the exact location for 991 of them by means of direction-finding techniques. From an analysis of whistle timing and location, he was able to identify cases in which whistles had received responding whistles from dolphins in other locations. Whistle matching, in which one dolphin responded immediately by repeating the signature whistle of another dolphin, was documented in 39 instances. The average distance between animals was 179 m (587 ft), and the maximum signature whistle and response observed between two animals was 579 m (2,000 ft). Imitating the vocalizations of other individuals was considered a key step in the evolution of language among humans. Because, other than humans, no land mammals were known to imitate sounds, study of the communication mechanisms and vocal interactions between dolphins offered a valuable opportunity to gain new perspectives on the origin of language and vocal learning. The presence of predators was known to be responsible for the evolution of certain traits, including a variety of behavioral and morphological mechanisms of defense, in prey organisms. Ann V. Hedrick of the University of California, Davis, conducted experiments on field crickets (Gryllus integer) to test the assumption of evolutionary models that the fitness advantage conferred to males that exhibit conspicuous female-attracting behaviour is offset by their greater risk of predation. Male crickets attract female mates by calling, and the length of time that different individuals call is genetically inherited. Female field crickets generally select male mates with the longest calling times. Predators of field crickets, which include mice, birds, lizards, and toads, are able to locate calling crickets by their sound, as are parasitoid flies that deposit their larvae on crickets. Consequently, individual crickets having longer periods of calling are more likely to attract female crickets but also are at greater risk of being located by predators and parasitoids. In experiments designed to compare how male crickets having different call lengths responded to predators, Hedrick used two measures of predator avoidance-the length of time before a male left a protected shelter after exposure to a predator and the length of time before it began to call again. The study demonstrated that males exhibiting the most conspicuous and effective behaviour to attract mates also were the most cautious in their response to predatory threats. This result contradicted the assumption that the males that are most ostentatious and thus most alluring to females necessarily suffer the greatest cost from predation. Rick A. Relyea and Earl E. Werner of the University of Michigan at Ann Arbor observed a morphological response of prey to the presence of predators that suggested an adaptive process. The predators in this case were larval dragonflies of the genus Anax, and the prey were tadpoles of four species of frogs of the genus Rana. In each of the prey species of frogs, the investigators observed an ability to alter morphological development that depended on whether dragonfly predators were present. To assess morphological change in individual tadpoles, they conducted computerized image analysis of tail-fin, body, and tail-muscle measurements. For each of the four species of frogs, tadpoles reared with dragonfly predators showed significant morphological differences from those raised without predators present, which indicated a potential for plasticity in body shape for each species. (By contrast, the normal rates of growth and development of the tadpoles of each species were not affected by predator presence.) Many of the changes noted by the investigators, such as the development of deeper tail fins that increase swimming speed, previously had been shown to be effective antipredator mechanisms that could possibly have adaptive value. Among the various ways that morphological differences within a species can be expressed is sexual dimorphism, in which members of the two sexes vary in body size or proportions and appearances of body parts. Charles Darwin gave three possible explanations for the evolution of sexual dimorphism. Two are sexual selection (selection for traits that improve mating success) and fecundity selection (selection for traits that increase reproductive output); in each case a reproductive advantage accrues to a particular sex. Examples of both are apparent in many species. Ethan J. Temeles and colleagues of Amherst (Mass.) College provided evidence in purple-throated carib hummingbirds (Eulampis jugularis) for Darwin's third, rarely documented explanation of sexual dimorphism-ecological causation. The carib hummingbirds on the island of St. Lucia in the West Indies pollinate two plant species, Heliconia caribaea and H. bihai, from which they obtain nectar. Male hummingbirds are larger and have longer wings than females, but the bills of females are more than 30% longer and are curved downward at twice the angle of the males' bills. In a census of foraging hummingbirds, all of 15 males were observed to feed on H. caribaea, compared with only 7 of 18 females, presumably owing to males' defending their territories. Instead, females fed primarily on H. bihai. The two flower species differ in floral structure, with the bills and feeding times of males being more compatible with H. caribaea and those of females with H. bihai. The investigators concluded that the evolution of bill dimorphism had been driven by responses to specialization for the different flower types. In a comparison of wing length to bill length among purple-throated carib hummingbirds and several of their close relatives, no reliable pattern was apparent that might have been expected from phylogenetic similarity, which suggested that sexual dimorphism in bill length had been influenced by behaviour or ecology of the species. Zoological conservation continued as an important issue for a variety of animal groups and species. R.N. Holdaway of Palaecol Research, Christchurch, N.Z., and Christopher Jacomb of the Canterbury Museum, Christchurch, examined information relating to the extinction of 11 species of moas, the enormous flightless birds formerly indigenous to New Zealand. The study provided the disquieting revelation that the elimination of all species had probably been completed within a century from the time of arrival in New Zealand of the Polynesian ancestors of the Maori, possibly as late as the 13th century. The investigators used human colonization rates and the human exploitation of birds, habitat loss, and numbers of birds initially present to develop simulation models to estimate the rates of decline. In order not to underestimate the time necessary for extinction to have occurred, the most conservative figures were used for each variable. Even when only 100 original colonists and a large original population of 160,000 moas were assumed and when the environmental impact of habitat loss was discounted, none of the models yielded a span of more than 160 years between the arrival of the Polynesians and the extinction of the birds. From a conservation perspective, it was significant that a small number of original colonists exploiting a long-lived animal species with a low reproductive rate could cause adult mortality rates high enough to render extinct a major portion of a region's fauna in a relatively short time. The applicability of the moa study to modern species was reinforced with the report by investigators from the University of Georgia's Savannah River Ecology Laboratory, Aiken, S.C., that documented the decline of representatives of all major groups of reptiles on all continents within the past century. As had been reported previously for amphibians, many reptile populations were unquestionably declining in size and abundance on a global scale. When coupled with the problems experienced by amphibians, the evidence suggested that a worldwide crisis was in progress. The causes of declines for both reptiles and amphibians were known with certainty in many instances and were suspect in many more, the six most commonly identified threats being habitat loss and degradation, introduced invasive species, environmental pollution, disease and parasitism, unsustainable commercialization, and global climate change. The study emphasized that the decline and disappearance of populations of reptiles and amphibians or, in some instances, of entire species can occur with little awareness even by biologists. The threats to these animals, as well as to other wildlife, had to be viewed as a serious worldwide situation not only by scientists but also by the general public and government policy makers. J. Whitfield Gibbons

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