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General Concepts on the Evolutionary Biology of Parasites Author(S): Peter W

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General Concepts on the Evolutionary Biology of Parasites Author(S): Peter W General Concepts on the Evolutionary Biology of Parasites Author(s): Peter W. Price Source: Evolution, Vol. 31, No. 2 (Jun., 1977), pp. 405-420 Published by: Society for the Study of Evolution Stable URL: http://www.jstor.org/stable/2407761 . Accessed: 29/08/2011 15:59 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. Society for the Study of Evolution is collaborating with JSTOR to digitize, preserve and extend access to Evolution. http://www.jstor.org GENERAL CONCEPTS ON THE EVOLUTIONARY BIOLOGY OF PARASITES PETER W. PRICE Department of Entomology, University of Illinois, Urbana, Illinois 61801 Received March 5, 1976. Revised August 9, 1976. Parasitism is a very common way of life, lation biology, evolutionary theory and and probably the prevalent means of ob- parasite biology. Third, predictions derived taining food among organisms. Adaptive from the general concepts act as a guide radiation among parasites has been exten- to critical characteristics of parasite biol- sive, and yet ecological and evolutionary ogy which need to be examined and tested concepts on parasitism are poorly devel- in natural populations. oped. Although Elton (1927) devoted a Much of the logic in this paper depends chapter in his pioneering ecology book to upon the interpretation of the word para- parasitism his conclusion was that the re- site. A distillation of views would be semblancesbetween predators and parasites lengthy, as no discrete limits to the para- are more important than the differences. sitic habit exist which are biologically This attitude is now prevalent in ecology meaningful (Askew, 1971; Kennedy, texts (e.g. Andrewartha and Birch, 1954; 1975). Therefore, I adopt what must be a Odum, 1971; Krebs, 1972; Colinvaux, generally accepted definition of a parasite, 1973), and although much attention is de- found in Webster's International Dictio- voted to predation, parasitism is almost ig- nary: "An organism living in or on another nored. Therefore, by using the inductive living organism, obtaining from it part or process, this paper attempts a synthesis of all of its organic nutriment, commonly ex- ecology and parasitology, the need for hibiting some degree of adaptive structural which has been recognized by Kennedy modification, and causing some degree of (1975), and it explores the evolutionary real damage to its host." Thus, an indi- implications of parasite ecology. vidual of any parasitic species will usually This synthesis should contribute to an gain the majority of its food from a single understanding of parasites in three ways. living organism in contrast to the more First, a reevaluation of the abundance of generalist browsers and predators which parasitic species is made. Arndt (1940) feed on many organisms, and saprophages estimated that 25% of animals in Germany which feed on dying or dead organic mat- are parasitic on others. Rothschild and ter. Although a parasitic species may uti- Clay (1952) stated that parasitic animals lize several host species, each individual probably exceed nonparasitic species in will exploit an individual host, and thus a number of species and individuals, but pro- single species. Parasites are specialists in vided little numerical support. A careful a host environment with close coevolution- quantitative evaluation by Askew (1971) ary ties. provided an estimate that 15% of insects, Most parasitologists include as parasites and 10% of all animal species are parasitic organisms such as mosquitoes, leeches, and insects. Calculations presented in this pa- ticks, having a brief relationship with a per indicate that well over 50% of the spe- host (e.g. Cheng, 1973). This convention cies of organismsextant today are parasitic. appears to be hardly justified by the defi- Second, general concepts on the ecology nition used above. However, parasitologists and evolution of parasites are presented, usually omit mention of parasites of plants. being derived from a combination of popu- Nematodes, fungi, bacteria, and many in- EVOLUTION 31:405-420. June 1977 405 406 PETER W. PRICE TABLE 1. Feeding habits of British insect species. There is debate on the placement of several large families such as the Carabidae. These beetles are normally considered predators, but many eat vege- table matter and others are saprophagous. As in this case when accurate placement is not possible the taxon has been omitted. Parasites Non-parasitic Order Predators herbivores on plants on animals Saprophages Thysanura 23 Protura 17 Collembola 261 Orthoptera 39 Psocoptera 70 Phthiraptera 308 Odonata 42 Thysanoptera 183 Hemiptera 123 283 5 Homoptera 976 Megaloptera 4 Neuroptera 54 Mecoptera 3 Lepidoptera 2,233 Coleoptera 215 65 909 18 1,637 Hymenoptera 170 241 435 5,342 36 Diptera 54 922 542* 1,672 Siphonaptera 47 TOTALS 665 415 5,941 6,262 3,646 %of insect fauna 3.9 2.4 35.1 37.0 21.5 Many species parasitic only as adults, e.g. Culicidae (49 sp.), Ceratopogonidae(135 sp.), Simuliidae (19 sp.). sects which feed in or on plants, fit the mology, plant pathology, botany, agricul- definition of a parasite. Day (1974) in- tural and forest entomology, and biological cludes these organismsin his book on host- control. parasite interactions. The majority of insect herbivores are parasitic. The large ABUNDANCE OF PARASITIC SPECIES order Homoptera, including leafhoppers, The froghoppers,aphids, coccids and whiteflies, proportion of organisms that are parasitic in any region is not is composed almost completely of parasitic easily esti- mated. Parasites are small, mostly well species. The larvae of the even larger or- concealed, and thus inconspicuous elements der, Lepidoptera, usually feed and mature of the flora and fauna. Few regional check on a single individual of the host plant lists of organisms are based on enough con- species, and gain a large percentage of the certed effort that would ensure an adequate total nutritional requirements for the or- sampling of both obvious and inconspicu- ganism's life span. In addition, parasitic ous species. One of the exceptions is the angiosperms are frequently ignored when fauna of the British Isles which is probably parasitism is discussed (Kuijt, 1969). the best documented fauna in the world, Therefore the parasitic habit is of con- because relatively intensive faunistic stud- cern to a variety of disciplines each con- ies have been conducted since the mid-18th tributing its perspective and knowledge to century. Thus it has been possible to com- the understandingof parasites. These dis- pile a check list of British insects (Kloet ciplines include parasitology, medical ento- and Hincks, 1945) which represents a EVOLUTIONARY BIOLOGY OF PARASITES 407 reasonably complete record of the largest for development of more sophisticated con- class of animals on the islands and in the cepts. The general approach will compare world. the ecology and evolution of parasites with I have counted the number of species in that of predators. each family of insects in Kloet and Hincks (1945) and classified as many families as Concept 1. Parasites are adapted to possible into the categories: predators, exploit small, discontinuous nonparasitic herbivores (mostly browsers environments. and pollinators, e.g. grasshoppers, bees), parasites on plants (e.g. thrips, bugs, cater- For a parasite each host exists in a pillars and some fly larvae), parasites on matrix of inhospitable environment (Wil- animals (e.g. lice, bed bugs, parasitic wasps liams, 1975). For very small organisms a and flies, and fleas), and saprophages (e.g. wide dispersion of resources makes col- many beetle and fly larvae). Of the 20,244 onizatiop of new hosts hazardous. Adapta- insect species listed in Kloet and Hincks, tions to reduce this hazard include: i) mass 16,929 can be readily classified into the production of spores or eggs (e.g. tape- above categories (Table 1). The remainder worms); ii) dispersal of inseminated fe- cannot be classified in this manner either males which form a high proportion of the because of diversity of feeding habits population (e.g. tetranychid mites, Mitch- within a family, or shortage of information ell, 1970); iii) dispersal by phoresy mak- on food eaten by larvae and adults. ing host discovery accurate (e.g. tarsone- The preponderanceof insects are classi- mid mites, Lindquist, 1969). In each of fied in the parasitic groups and represents these cases a single female can found a col- 72.1% of the insect fauna (Table 1). Pred- ony on a new resource remote from its ators account for only 3.9% of insects in origin. Multiplication in the colonizer's Britain by this method. Even if a con- progeny may lead to a new and relatively servative estimate is made by assuming all isolated population. New propagules col- the parasites in the fauna have been identi- onize other isolated resources. Thus para- fied in my classification they represent sites tend to exist in small homogenous about 60% of the insects. Since about three populations with little gene flow between quarters of the known animals on earth them (see also Jones, 1967). are insects, an estimate that parasitic in- Types of reproductionin parasites which sects represent close to half the animals on permit a single female to found a new pop- earth does not seem unrealistic. When ulation include inbreeding among prog- other large groups of parasitic animals eny (e.g. parasitic wasps; Askew, 1968), hermaphroditism (e.g. trematodes, ces- found among the nematodes, copepods, todes), or asexual reproduction (poly- flatworms, ticks, mites and protozoa, are embryony in digenetic trematodes and par- added to the numbers of parasitic insects it asitic wasps, parthenogenesis in many is clear that parasitism as a way of life taxa).
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