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PERSPECTIVES

ECOLOGY

Domestication has had higher success rates Rapid Domestication of in the sea relative to those seen in the long history of land ’ domestication. The rise Marine Species of aquaculture has global consequences. Carlos M. Duarte, Nùria Marbá, Marianne Holmer

bout 11,000 years ago, 100 for future domestication. began to do- LAND Second, the greater Amesticate plants and diversity of life forms in animals (1–3). In the next 9000 the ocean compared to years, hundreds of land species those on land provides a and a few aquatic species were 80 broader range of opportu- domesticated. Since then, how- nities for domestication. ever, few land species have been The limited success in do- MARINE PLANTS domesticated. In contrast, the mesticating land animal domestication of aquatic— species has been attrib- 60

particularly marine—species has domesticated uted to the paucity of suit- grown exponentially. Aquacul- able species: Many land ture is emerging as a revolution plants are poisonous or species LAND ANIMALS in of global impor- toxic to humans, and many total tance to humankind. 40 land animal species have on June 20, 2008 Domestication of wild spec- of slow growth and long ies to produce food means that life cycles, specialized Percent the breeding, care, and feeding MARINE ANIMALS diets, or adverse behav- of are controlled ioral traits (3). by humans (4). By 2000 years 20 Third, aided by the ago, an estimated 90% of the rapid spread of technical species presently cultivated on and scientific knowledge, land had been domesticated. FRESHWATER ANIMALS domestication of aquatic

Since the , species is developing glo- www.sciencemag.org the increase in the numbers of 0 bally, whereas land species 100,000 10,000 1000 100 10 1 domesticated land and Time (years before present) were domesticated in just animal species has been mod- a few regions (1–3). A est (~3%) (see the figure). Land versus water. Most land species were domesticated earlier than aquatic species, but in similar global effort to do- In contrast, the rise of aqua- the past 100 years, many more aquatic species than land species have been domesticated (6). mesticate additional land culture is a contemporary phe- animal species is preclud- nomenon (5). About 430 (97%) of the aquatic species and 0.0002% of known land animal ed by the paucity of candidate species and the species presently in culture (see the table) species have been domesticated(7), compared lack of market demand. Downloaded from have been domesticated since the start of the with 0.17% of known marine plant species The domestication of an aquatic species 20th century, and an estimated 106 aquatic and 0.13% of known marine animal species. typically involves about a decade of scientific species have been domesticated over the past Effective genetic improvement programs for research (13). Current success in the domesti- decade (see the figure) (6). The number of many aquaculture species (8) should be facili- cation of aquatic species results from the 20th- aquatic species domesticated is still rising rap- tated by their huge reproductive output and century rise of knowledge on the basic biology idly (see the figure) (6). Even allowing that the short generation times compared to those of of aquatic species and the lessons learned from rates for early domesticates are estimates, domesticated land animals. past success and failure. The domestication of aquatic domestication rates are ~100 times as There are several reasons for this contrast aquatic species also involves fewer risks than fast as the rates of domestication of plant between the success in the domestication of that of land animals, which took a large toll in and animal species on land over the period land and marine animal species. First, land lives through diseases transferred from when domestication was fastest (see the table) domestication has drawn largely from mam- (3); no human pathogens of comparable (6). Despite a vastly longer history, the domes- mals and , with few (such virulence have yet emerged from aquaculture. tication of land species has been less success- as bees and snails) domesticated. In contrast, a The stagnation in the world’s fisheries and ful than that of marine species (7), particularly diverse array of marine taxa—including mol- overexploitation of 20 to 30% of marine fish for animals: 0.08% of known land plant lusks, , vertebrates, , species (11) have provided additional impetus jellyfish, and worms—have been domesti- to domesticate marine species, just as overex- C. M. Duarte and N. Marbá are at IMEDEA (CSIC-UIB), cated (9, 10). Many more wild marine species ploitation of land animals provided the impe- Instituto Mediterráneo de Estudios Avanzados, 07190 are used as food [more than 3000 marine tus for the early domestication of land species Esporles, Mallorca, Spain. E-mail: carlosduarte@imedea. uib.es M. Holmer is in the Institute of Biology, University species compared to fewer than 200 land (2). Aquaculture production has been growing of Southern Denmark, 5230 Odense M, Denmark. species (9, 11, 12)], providing further scope at rates of ~7 to 8% per year (5), compensating

382 20 APRIL 2007 VOL 316 SCIENCE www.sciencemag.org Published by AAAS PERSPECTIVES for the stagnation of fisheries, and is likely to Global pace of species domestication become the main source of marine food for Time since domestication humans as demands continue to grow. Number of Specific growth (years before present) in the number of The broad range of domesticated marine Species group species 50% species 90% species domesticated species domesticated –1 species helps to integrate the production domesticated domesticated (% year ) across trophic levels, thereby maximizing Land plants 250 4000 2000 0.026 (76) output while decreasing environmental im- Land animals 44 5000 146 0.014 (30) pact (14). It also increases the range of Freshwater animals 180 22 4 3.4 (180) marine habitats where aquaculture can be Marine animals 250 19 4 3.3 (250) conducted, and diversifies food sources and Marine plants 19 32 <10 2.5 (19) generates a wide range of market prices for Rates of change. The numbers of presently domesticated species, the times by which 50% or 90% were aquaculture products. However, aquaculture domesticated, and the rates of domestication differ widely between land and aquatic species. In the last col- development also has negative consequences umn, the specific growth in the number of domesticated species is defined as the percent increase in the num- for the environment and biodiversity, includ- ber of species domesticated per year over the period of fastest domestication rates (6); the number of species ing deterioration of coastal ecosystems by for which domestication dates were available is given in parentheses. aquaculture effluents and impacts on wild species used as feed (15). The continuity of ify employment and livelihood patterns of Dissemination of Global and Regional Fishery Statistics. FI Programme Websites (UN Food and Agriculture present rates of domestication and the capac- those involved in this . The growth in Organization, Rome, 2006); see www.fao.org/fi/default.asp. ity of aquaculture to meet the rising demands the domestication of marine biodiversity thus 10. P. J. W. , Hydrobiologia 402, 175 (1999). for seafood of a growing human population represents a fundamental change in the way 11. FAO, FAOSTAT-Agriculture (UN Food and Agriculture Organization, Rome, 2006); see www.faostat.fao.org/ require that, by minimizing environmental humans relate to the oceans. default. aspx. impact, a sustainable model be achieved. 12. R. S. V. Pullin, in Biodiversity, Science and Development: References and Notes Domestication should aim at closed produc- Toward a New Partnership, F. Di Castri, T. Younes, Eds. 1. D. Normile, Science 275, 309 (1997). (Cambridge Univ. Press, Cambridge, UK, 1996), tion cycles, where feed is produced in the 2. A. M. Mannion, Progr. Phys. Geogr. 23, 37 (1999). pp. 409–423. on June 20, 2008 farm and the target organisms reproduce and 3. J. Diamond, Nature 418, 700 (2001). 13. L. Curry Woods III, Aquaculture 202, 343 (2001). 4. E. B. Hale, in The Behaviour of Domestic Animals, E. S. E. 14. A. Neori et al., Aquaculture 231, 361 (2004). grow from egg to adult in culture, reducing Hafez, Ed. (Bailliere, Tindall and Cassell, London,1969), 15. R. L. Naylor et al., Science 282, 883 (1998). pressures on wild stocks. pp. 22–42. 16. Supported by the projects SAMI and MarBEF Network of The increase in aquaculture has global con- 5. FAO, of World Aquaculture: 2006. FAO Fisheries Excellence, funded by the European Commission. We are Technical Paper. No. 500. (UN Food and Agriculture indebted to Y. Olsen and D. Soto for insights and com- sequences, both as a food source and in terms Organization, Rome, 2006); see www.fao.org/ ments that have greatly improved this work, J. Guieu for of environmental implications. The develop- fidefault.asp. help in compiling data, and S. Agustí and S. Zanuy for 6. Materials and methods are available as supporting mate- helpful suggestions. ment of aquaculture is bound to replace fish- rial on Science Online. eries as replaced on 7. B. Groombridge, M. D. Jenkins, Eds., Global Biodiversity: Earth’s Living Resources in the 21st Century (World Supporting Online Material land. This should help release pressure on www.sciencemag.org Conservation, Cambridge, UK, 2000). Materials and Methods increasingly scarce freshwater resources used 8. P. Sorgeloos, World Aquaculture 30, 11 (1999). Table S1 to produce food on land, and stimulate techno- 9. FAO, Fishstats. FAO Fishery Information, Data and References logical developments. These changes will mod- Statistics Unit (FAO-FIDI). 2004—Collation, Analysis and 10.1126/science.1138042

EVOLUTION

Aging of male organisms and of their sperm Downloaded from reduces fertility and embryo viability, leading Aging and Sexual Conflict to evolutionary conflict between the sexes. Rebecca Dean, Michael B. Bonsall, Tommaso Pizzari

n many human societies, men are becom- on the evolutionary conflict between sexual study demonstrates that the fertilizing ability ing fathers increasingly late in life, and it partners, known as sexual conflict. of an ejaculate peaks at an intermediate Iis estimated that fertility problems expe- Male fertilizing efficiency is especially male age. Most young males copulated with rienced by one-third of couples can be attrib- important in species where females mate females but only 36% of them had developed uted to male factors, including aging (1). with multiple males and the ejaculates of mature sperm, indicating that most young Aging can affect male reproductive success different males compete for fertilization, a males were not sexually mature. Similarly, through two processes, each with distinct process called sperm competition. One although all old males produced mature evolutionary implications: the age of the recent study of the hide beetle (Dermestes sperm, some of them failed to transfer sperm male and the age of his sperm. Recent empir- maculates) (2) reveals that male aging may during mating (aspermic copulation). Males ical studies demonstrate that both male aging be an important determinant of the outcome in their prime (intermediate age), on the and sperm aging may have a dramatic impact of sperm competition. The study analyzed other hand, never failed to inseminate a on fertility, embryo viability, and ultimately fertilization success in two scenarios: when female. Moreover, in sperm competition, the ejaculates of two males were inseminated their ejaculates outcompeted those of old and into a female (sperm competition), and when young males in fertilizing the eggs of a The authors are at the Edward Grey Institute, Department of , University of Oxford, Oxford OX1 3PS, UK. the ejaculate of only one male was insemi- female. These results confirm earlier work E-mail: [email protected] nated (absence of sperm competition). The on this species showing that a female incurs

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