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General Concepts on the Evolutionary 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

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http://www.jstor.org GENERAL CONCEPTS ON THE OF PARASITES

PETER W. PRICE Department of , 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 among . 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 are poorly devel- in natural populations. oped. Although Elton (1927) devoted a Much of the logic in this paper depends chapter in his pioneering 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 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 , parasitism is almost ig- nary: "An 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 , 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 ." Thus, an indi- implications of parasite ecology. vidual of any parasitic 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 of generalist browsers and predators which parasitic species is made. Arndt (1940) feed on many organisms, and saprophages estimated that 25% of 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 - quantitative evaluation by Askew (1971) ary ties. provided an estimate that 15% of , Most parasitologists include as parasites and 10% of all species are parasitic organisms such as mosquitoes, , and insects. Calculations presented in this pa- , having a brief relationship with a per indicate that 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 . being derived from a combination of popu- , fungi, , and many in-

EVOLUTION 31:405-420. June 1977 405 406 PETER W. PRICE

TABLE 1. Feeding habits of British species. There is debate on the placement of several large families such as the Carabidae. These 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 on plants on animals Saprophages Thysanura 23 Protura 17 Collembola 261 Orthoptera 39 Psocoptera 70 Phthiraptera 308 Odonata 42 Thysanoptera 183 123 283 5 Homoptera 976 Megaloptera 4 54 Mecoptera 3 2,233 Coleoptera 215 65 909 18 1,637 170 241 435 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, , 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,, 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- 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 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, ), parasites on plants (e.g. thrips, bugs, cater- For a parasite each host exists in a pillars and some larvae), parasites on matrix of inhospitable environment (Wil- animals (e.g. lice, bed bugs, parasitic liams, 1975). For very small organisms a and , and ), and saprophages (e.g. wide dispersion of resources makes col- many and fly larvae). Of the 20,244 onizatiop of new hosts hazardous. Adapta- insect species listed in Kloet and Hincks, tions to reduce this include: i) mass 16,929 can be readily classified into the production of or (e.g. tape- above categories (Table 1). The remainder ); 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 , 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, , todes), or asexual (poly- , ticks, mites and , 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). The commonnessof parthenogenesis is more common than all other feeding among parasitic arthropodsis not generally strategies combined. appreciated. Arrhenotoky (the production of males from unfertilized eggs) occurs in ECOLOGICAL AND EVOLUTIONARY all Hymenoptera, probably the majority of CONCEPTS Thysanoptera, many iceryine and aleurodid The following concepts are grouped as a Homoptera, and in some Coleoptera start to the synthesis of evolutionary biol- (White, 1973). It is a major mode of re- ogy and parasitology. The concepts are production in certain families of mites necessarily basic in order to retain gener- (Oliver, 1971). Thelytoky (the production ality, but they may form the ground work of females from unfertilized eggs) occurs 408 PETER W. PRICE

TABLE 2. Number of species in the ten largest families in the British insect fauna in each of the categories listed. Primary parasites feed on plants and secondary parasites feed on animals. Families marked with an asterisk contain some or all members reproducing through parthenogenesis. The family Cynipidae contains some secondary parasites.

Predators Primary Parasites Secondary Parasites

Dytiscidae 110 Cicidomyiidae* 629 Ichneumonidae* 1938 Sphecidae* 104 Curculionidae* 509 * 891 Coccinellidae 45 Aphididae* 365 Pteromalidae* 493 Corixidae 32 Tenthredinidae* 358 Eulophidae* 485 Cucujidae 32 298 228 Hemerobiidae 29 Chrysomelidae 248 176 Vespidae* 27 Cicadellidae 242 Lamprotatidae* 156 Asilidae 26 Cynipidae* 238 Platygasteridae* 147 Anthocoridae 25 Olethreutidae 216 Encyrtidae* 144 Soldidae 20 Miridae 186' Diapriidae* 125 MEAN 45 MEAN 329 MEAN 478 sporadically in a great variety of insects eny of a single female are likely to be more (Suomalainen, 1962) and cyclical par- uniform than progeny from females pro- thenogenesis (i.e., heterogonic life cycles, ducing fertilized eggs (Mayr, 1963; White, Williams, 1975) is prevalent in aphids 1970; Williams, 1975). However, this dis- (Aphididae) and wasps (Cvnipidae), advantage can be reduced by utilization of and it occurs in gallflies () highly stable and predictable microenviron- (Suomalainen, 1962; White, 1973), and ments provided by the homeostasis of liv- many parasites in other taxa (Williams, ing organisms. A positive feedback may 1975). Thus parthenogenesisoccurs in five reinforce the evolution of parthenogenesis of the ten largest families of parasitic in- in parasitic organisms (Fig. 1). 3. The sects on plants in Britain (Table 2): Cec- gross reproductive rate of thelytokous fe- idomyiidae, Curculionidae, Aphididae, males is doubled (White, 1973; Williams, Tenthredinidaeand Cynipidae (see Suoma- 1975), so the probability of finding a new lainen, 1962). In the animal parasites of host is similarly increased. 4. Particularly the British fauna eight of the largest fami- adaptive combinationsof genes are fixed in lies have all species parthenogenetic since perpetuity in thelytokous multiplication: they are within the order Hymenoptera: automictic thelytoky tends to produce Ichneumonidae, Braconidae, Pteromalidae, homozygous individuals while apomictic Eulophidae, Lamprotatidae, Platygasteri- thelytoky involves mitotic divisions only dae, Encyrtidae, and Diapriidae (Table 2). (White, 1973). This locking of gene com- Parthenogenesis is so common in para- binations may be especially important in sites and yet its adaptive nature for parasitic organisms where large banks of parasites is not well understood. Some genes are likely to be involved with close adaptive features follow: 1. A single fe- coevolutionary tracking of the host system male can establish a new colony (White, (see Fig. 1). Disruption of such a block 1973; Williams, 1975), and multiplication would generate gross maladaptions with al- can occur when the probability of contact most certain lethal results. between more than one individual of the Parthenogenesisis relatively rare in pred- same species is very low (Tomlinson, atory taxa such as Odonata, Heteroptera 1966). 2. Parthenogenetic parasites may and spiders (White, 1973). Of the 10 larg- seem to be maladapted to a patchy, com- est families of predators in the British in- plex and changing environment since prog- sect fauna only the two hymenopterous EVOLUTIONARY BIOLOGY OF PARASITES 409

PARTHENOGENESIS

ASEXUALREPRODUCTION PRESERVATIONOF REDUCEDVARIABILITY IS ADAPTIVE LARGE GENECOMPLEXES OF PROGENY ISADAPTIVE ESSENTIAL

PROBABILITYOF FINDING MANYBLOCKS OF GENES REDUCEDFITNESS IN MATESIS LOW INVOLVEDWITH COEVOLUTION UNPREDICTABLE ENVIRONMENT WITHHOST

HOSTSPATCHILY USE OF MICROENVIRONMENT DISTRIBUTEDIN SMALL - PROVIDEDBY LIVING POPULATIONS ORGANISMSIS ADAPTIVE

FIG. 1. The positive feedback loop which may promote the evolution of parthenogenesis among parasitic organisms or at least permit it to exist. It is assumed that parthenogenetic species may revert back to under favorable selection pressure.

families, Sphecidae and Vespidae, show any be more frequent than polymorphism with form of parthenogenesis (cf. Suomalainen, the population structure as envisioned here. 1962; White, 1973). Specialization permits a relatively large number of species to pack into a given set Concept 2. Parasites represent the of resources so many species may coexist extreme in the exploitation of coarse- under equilibrium conditions. grained environments. In contrast to parasites, predators are relatively large and mobile and exploit a The small size of parasites, the specific relatively fine-grained environment. Hab- cues used in discovery of relatively large itat differences are small compared to the food items (e.g. Vinson, 1975), and the tolerance of the animals. Levins (1962) poor mobility of many stages in the life cy- predicted that such populations will be cle means that they must exploit a coarse- monomorphic and unspecialized, with geo- grained environment in the sense of Mac- graphic patterns showing continuous clines. Arthur and Levins (1964) and MacArthur Few of these generalists can coexist under and Wilson (1967). Such small organisms, equilibrium conditions. which face relatively large differ- ences to the tolerance of indi- compared Concept 3. Evolutionary rates and in viduals may respond two ways to en- speciation rates are high. vironmental variability (Levins, 1962). If the environment is stable in time and vari- The environmental constraints on the able in space, Levins predicts that the parasitic habit described in Concepts 1 and population should be monomorphic and 2 promote the fractionation of gene pools specialized with a geographic pattern of and produce an advantage to inbreeding or discrete races. If the environment is uni- asexual reproduction. They foster rapid form in space and variable in time the pop- divergence of populations, formation, ulation should be polymorphic, with spe- and eventual speciation. Short life cycles, cialized types, and have a geographic short generation times and high fecundity pattern of clines in frequencies of these result in high reproductiverates which per- specialized types. Since hosts probably mit dramatic changes in represent a variable resource both in time and rapid differentiation of populations un- and space the development of both geo- der dissimilar selective regimes. Predom- graphic races and polymorphism in para- inantly homozygous populations (or hap- sites may be common, although races will loid males in parasitic Hymenoptera) have 410 PETER W. PRICE all genes exposed to selection in each gen- concept of high evolutionary and speciation eration. Both the founder effect and ge- rates. Even though some parasitic taxa netic drift are probably significant in evolved much later than some predatory speciation of parasites. Both Wright (1940, taxa, families of parasites on plants are 1943, 1949) and Carson (1968, 1975) have on average almost eight times larger than explored the evolutionary potential of pop- those of predators, and families of para- ulations with this structure and they con- sites on animals are over ten times larger. cluded that the probability of evolution In both groups of parasites the tenth fam- and speciation was much higher than in a ily is larger than the first ranked family of randomly breeding population of the same predators. size. Evidence for high evolutionary rates Concept 4. Adaptive radiation is may be seen in the many sibling species, extensive and its degree of development subspecies, host races, and different types in each taxon of parasites depends upon observed in parasitic organisms (e.g., a) the diversity of hosts in the taxon or Thorpe, 1930; Mayr et al., 1953; Brown, taxa being exploited (i.e., numbers of spe- 1959). Mayr (1963) states that sibling cies and the degrees of difference between species are especially common among in- species) sects and singles out the Lepidoptera, Dip- tera, Coleoptera and Orthopteraas provid- b) the size of the host target available to potential colonizers (body size, popula- ing abundant examples. In the Coleoptera tion size, geographical distribution) he notes that sibling species are particu- c) the evolutionary time available for larly common in the Curculionidae,Chrys- colonization of hosts omelidae, and Cerambycidae, three of the the selective coevolution- largest families in the order with the ma- d) pressure for ary modification (i.e., for specialization) jority of species parasitic on plants. Zim- the of hosts. merman (1960) suggests that five or more e) mobility new species of Hedylepta (Lepidoptera) To understand the evolution of the large must have evolved within 1000 years in numbers of parasite species part of the Hawaii since they are endemic and spe- answer can be found in an understanding cific to banana which was only introduced of why there are so many resources avail- that long ago. Roelofs et al. (1972) and able and what influences the presence or Klun et al. (1973) describe the sibling absence of parasites on these resources. species of the corn borer which respond to Some of the factors are treated in this sec- different isomers of the otherwise identical tion. pheromones. Bush (1975a) states that a Diversity of hosts.-Adaptive radiation new race of the western cherry fruit fly can be most extensive when many related (Rhagoletis indifferens) was extant on do- species of host are available for coloniza- mestic cherry within 89 years of the plants' tion, particularly if the hosts within a taxon introduction to Northwest North America. differ in an important way relative to the Jones (1967) discusses the several types of requirements of the parasites. Many ex- caused by biologically dis- amples could be given of a fairly weak re- tinct forms within each of the species lationship between size of family of hosts donovani and L. tropica. He and numbers of parasites that exploit mem- also suggests on theoretical grounds that bers of that family. For example, there are speciation can occur in one generation, a more of the leaf mining flies in the family view held by Bush (1974, 1975a, b) based Agromyzidae on large families of plants on studies of herbivorousparasites. than small families (Fig. 2). However, the The large size of many families of para- regression accounts for only 61% of the sitic insects (Table 2) also supports the variation and much of the remaining scat- EVOLUTIONARY BIOLOGY OF PARASITES 411

50

Co

z 40 -J *Gr

c,30 ,, 0lJ Ra , ' LiAJ 0 -0 j2 O ,,- Cn Urn,'~ -- eRo -4 0~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~020 0, ,

0I 0 0 Sc"0*L < SE Co Um ,,".a ,,' C *Ro o 0 - ? ? SC, o Le

t ,0LaII . zrz so'Sa- ,, '.0 ..y

0 100 200 300 400 500 600 700 NUMBER OF PLANT SPECIES PER FAMILY

FIG. 2. Relationship between number of species in each plant family (from Fernald, 1950) and the number of agromyzid flies attacking each family in Canada and Alaska (from Spencer, 1969). For those plant families attacked by more than five agromyzid species (above small dashed line) the fol- lowing symbols are used: (open circle) agromyzids monophagous, (closed circle) agromyzids oligoph- agous, (closedlopen) some monophagous and other oligophagous, (open|closed) only two genera in family. Sa-Salicaceae, Ca-Caprifoliaceae, Um-Umbelliferae, Ra-Ranunculaceae, Sc-Scrophulariaceae, La-Labiatae, Le-Leguminoseae, Gr-Graminae, Cy-Cyperaceae, Ro-Rosaceae, Co-Compositae. The re- gression line is described by the formula Y = 0.7648 + 0.0455X (r2 = 0.61, P < .01). ter is probably accounted for by the chem- perhaps because of the exceptional com- ical diversity of plants in each family. monness of species and individuals making Where species in a family are chemically colonization more probable. The example distinct, for example in secondary metab- of the Agromyzidae supports Eichler's olic products, or as Hering (1951) noted, (1948) rule, well known to parasitologists, in plant , parasites are predom- which states (from Noble and Noble, inantly monophagous (i.e., feed on host 1971): "When a large taxonomic group species within a single genus). Parasites (e.g., family) of hosts consisting of wide utilizing hosts in families of low chemical varieties of species is compared with an diversity tend to be oligophagous (i.e., feed equivalent taxonomic group consisting of on species in several genera). Monopha- few representatives, the larger group has gous species have a narrow feeding niche, the greater diversity of parasitic fauna." therefore many species can pack onto a At each successive the di- given number of host species relative to versity of potential hosts increases and the oligophagous parasites. Only the family opportunities for adaptive radiation ex- Graminae is an exception to this pattern, pand, within the limits discussed below. 412 PETER W. PRICE

trophic level in a parasite (e.g., 40- the obligate of ) resources i *Be may be so dispersed and hard to 0 find that a trend towards generalization, Q and reduced numbers of species, might be w expected (Darwin, 1872; Janzen, 1975). The resulting or- 0~L~ 30 diversity of parasitic (I) ~ ~ ~ ~ ~ ~ ~ ~ C ganisms supported after the evolution of a new genus or species may be impressive. An extreme case is seen in the genus Quer- 0~ Ro cus where even in the small fauna of Brit- 20 ain the supports at least 390 species of parasitic herbivores (Barnes, 1951, 1955; Southwood, 1961; Darlington, 1974; Askew, 1975; and Morris, 1974 provide 0 ~ ~ ~ ~ ~ ~~~~~1 numbers of species in various taxa). The 0~~~~~~~~~~~~~~~~~~~~0 Mz~~~~~~~~ 10- A) 1 c number of secondary parasites supported by these herbivores must be even higher. z The , Operophterabrumata, is <~~~~~~~~ known to support 63 species of parasite Ro-. yRo (Embree, 1971) and microlepidoptera in 0 HERBS SHRUBS the genus Phyllonorycter may support about 50 species of parasitic insects FIG. 3. Relationship between plant form of a (Askew, 1975). family and the average number of microlepidop- Size of host target.-The large number tera per plant species attacked in each family. of parasites which coexist on is possi- Host species from Ford (1949). Ol-Oleaceae, Ro- Rosaceae, Be-Betulaceae, Fa-Fagaceae, Ul-Ulma- ble partly because of the 's large size. ceae, Co-Corylaceae, Ac-Aceraceae. Open circles The many resources available for coloniza- = the mean number for each plant form. Dashed tion and the species that exploit them have line = the trend of increased parasites per plant been described by Morris (1974). The species as plant size increases. Mean number of average numbers of microlepidoptera per leafmining Lepidoptera per plant genus for each plant form = large closed circles. Solid line = species in a family of plants are much less trend per plant genus. Host species from Hering limited in trees than in shrubs and much (1957). Families with representatives in more less in shrubs than in herbs (Fig. 3). Leaf than one plant form were subdivided, as shown mining Lepidoptera, Coleoptera and Hy- for the Oleaceae and Rosaceae. The large range in numbers of species on trees is discussed in Concept menoptera illustrate similar trends when 4c. Hering's (1957) keys are analyzed. A sim- ilar response may be observed among ecto- parasites (e.g., lice, Mallophaga, and Thus, primary parasites (parasitic herbi- feather ticks, Sarcoptiformes) of , vores) may be abundant, with many large with large birds having more regions of the families included, but radiation has been body which are sufficiently distinct so that even more extensive in the largest families different parasites can colonize and main- of secondary parasites (parasitic carni- tain a competitive edge in each region vores) (Table 2). The family Ichneumoni- (Dogiel, 1964). For example, in an exten- dae is over three times larger than the sive survey Foster (1969) discovered three largest family of primary parasites in the species of mallophagan which occupied two British fauna, and Townes (1969) esti- regions of the body on the orange-crowned mates a total of about 60,000 species must warbler, Vermivora celata, whereas Dub- exist in the world. Only at the fourth inin (in Dogiel, 1964) found seven species EVOLUTIONARY BIOLOGY OF PARASITES 413 on the larger Ibis falcinellus located in four Phthiraptera; Lindquist, 1969, on Acarina; distinct body regions. see also Mayr et al., 1953; Mayr, 1963, for Host population size as well as the geo- use of parasites to distinguish sibling spe- graphic distribution of a species are equally cies in the host group). Such diverse important in determining the probability groups as beetles on pines, termitophiles in of a parasite reaching a new host, coloniz- colonies, and on turbel- ing it and maintaining a lasting relation- larians have provided clues to inconspicu- ship with the host. Large populations and ous differences between hosts. This con- extensive range of a potential host must in- cept has been formalized into a rule by crease the chances of colonization by para- Fahrenholz: common ancestors of present- sites (Strong 1974a, b; Strong and Levin, day parasites were themselves parasites of 1975). Perhaps Kellogg (1913) was the the common ancestors of present-day hosts. first to regard hosts as islands. Janzen Degrees of relationship between modern (1968, 1973) also points out that hosts can parasites thus provide clues as to the par- be regarded as islands available for col- entage of modern hosts (Noble and Noble, onization by parasites and they are there- 1971). The more specific Fuhrman's rule fore subject to the insights of the theory of (Dogiel, 1964), that each order of birds island (MacArthur and Wil- has its particular cestode fauna, implies a son, 1967), as Dritschilo et al. (1975) have similar relationship between the evolution demonstrated for species on cricetid of host and parasite. rodents in North America. Probability of Selective pressure for coevolutionary colonization is influenced by island size modification.-The importance of interac- which can be regarded as host size, host tion between host and parasite in the evo- population size or range size. lution of both has been stressed by numer- Evolutionary time available.-In the ous authors (e.g., Brues, 1924; Hegner, previous section trees were shown to sup- 1927; Dogiel, 1964; Ehrlich and Raven, port on average more parasitic herbivores 1964). The stepwise coevolutionary pro- than herbs (Fig. 3). However, the range cess results in extreme specialization and in average numbers of parasites per species complex defense mechanisms (e.g. Whit- of tree is extreme and is not accounted for taker and Feeny, 1971). As described in by the size of the host individuals. Most Concepts 2 and 3 specialization is likely to of this range can be explained by the rela- increase the rate of speciation which may tive evolutionary opportunity provided by occur in both host and parasite. Indeed, each species of tree. Common trees which as Atsatt (1973) points out, parasites may have existed in a region over considerable have increased the adaptive potential of spans of time have high numbers of para- their angiosperm hosts enabling the evolu- sites whereas recently available hosts with tion of heterotrophic species, including the a restricted range have small numbers parasitic flowering plants. (Southwood, 1961; Opler, 1974). The importance of coevolutionary pres- Once parasites have colonized a host, di- sure was illustrated in the relationship be- vergence of host stock and eventual specia- tween agromyzid leaf miners and plants tion leads to divergence of the parasites (Fig. 2). Families containing species which and, depending on the time involved, re- are biochemically distinct had relatively sults in host-race formation or new parasite high numbers of agromyzids which were species. Thus parasites can be extremely also specialists. This is seen particularly useful in elucidating the phylogenetic rela- clearly when host ranges are compared for tionships of their hosts (Jordan, 1942, on agromyzid leaf miners on Graminae and Siphonaptera; Harrison, 1914; Metcalf, Umbelliferae. The latter family is com- 1929; Hopkins, 1942, 1949; Clay, 1950, on posed of aromatic plants which produce a 414 PETER W. PRICE

50 - 18 U) Umbelliferae

z 0- 40 - 12 ,,,o__y U) o Grominae H12- z >- 30 0 or \Umbelliferoe (-9 c-?6 -\ < 20 06~~~~~~~~~~~~~ 0

rnLUI 10- o0 Graminae 0 1 2 4 8 16 z N0 PARASITENUMBER CLASS

0 I 2 4 8 16 32 64 128 FIG. 5. Frequency distribution of the number HOST NUMBERCLASS of parasitic agromyzids per genus of plants in the families Graminae and Umbelliferae. Parasite FIG. 4. Frequency distribution of the number number classes arranged on a logarithmic scale as of genera attacked by agromyzid parasites in the in Figure 4. Data are from an analysis of keys host plant families Graminae and Umbelliferae. on leafminers in Europe by Hering (1957). Host number classes on a logarithmic scale with the first number in the class given. Thus class 8-15 = 8. Data are from an analysis of keys on leafminers in Europe by Hering (1957). sures. Thus for specialization are reinforced, isolation of populations be- comes more likely, and speciation is more rapid. As Mayr (1963) expresses it, "Host diverse array of essential oils and related resins (Hegnauer, 1971) with a large num- specificity is thus an ideal prerequisite for rapid speciation" (see also Ross, 1962). ber of pharmaceutically interesting species The end result is a comparatively large (Heywood, 1971). Although the Umbellif- number of specialists attacking the Umbel- erae is a much smaller family than the liferae whereas many more generalists at- Graminae many more agromyzid species tack the Graminae. attack members of the family in Europe The degree to which specialization is de- (61 species on Umbelliferae, 35 species on manded is a potent force in adaptive radia- Graminae; from analysis of keys by Her- ing, 1957). This is apparently because the tion. Szidat's Rule (Eichler, 1948) states that the more specialized the host group, chemical diversity of potential hosts within the more specialized are its parasites; and, the Umbelliferae has forced specialization conversely, the more primitive or more of the parasites and 82% of the species of generalized the host, the less specialized agromyzid attack only one genus each; are its parasites. Hence, the degree of spe- they are monophagous (Fig. 4). In con- cialization may serve as a clue to the rela- trast only 29% of agromyzids are monoph- tive phylogenetic ages of the hosts (as agous on grasses. In addition, there are fewer agromyzids on each genus of Umbel- stated by Noble and Noble, 1971). Pred- liferae than of Graminae (Fig. 5). No ators must remain generalized and radia- more than seven species occur on any one tion has been unimpressive (Table 2). genus in the former family and 15 genera Plant parasites show varying degrees of have only one parasite species. When there radiation depending on the intimacy of are few parasite species per host, coevolu- their association with the host. Plant bugs tion can proceed rapidly since adaptive re- (Miridae) are mobile, relatively large ecto- actions need not be compromised by con- parasites, although immature stages spend flicting adaptations in response to other much time on a single host. In the British parasites exerting different selective pres- fauna 186 species have been identified. EVOLUTIONARY BIOLOGY OF PARASITES 415

The much smaller plant lice (Aphididae) plant host's and the associated are more sessile, more intimately associated parasite's . After prolonged co- with the host and have undergonemore ex- evolution, where the stepwise process has tensive radiation (365 species in British escalated defenses many times, many such fauna). Some are gall-makers (Eastop, complementary gene-for-gene pairs must 1973). The largest families of plant para- exist between parasite and host. This com- sites are predominantly endoparasitic. The plex of genes coadapted to counterparts in weevils (Curculionidae) as larvae mine in the host, like the closed variability system leaves, under , in or , or described by Carson (1975), must be feed in rolled leaves, fruits and seeds. maintained or is reduced drasti- They number 509 species. The most highly cally. These blocks of genes may be main- coevolved parasitism occurs in the gall- tained by inversions, development of super- forming endoparasitic flies, Cecidomyiidae, genes, or by cloning, the last so often seen which are also the most numerous (629 in parasitic organisms (see Concept 1). species) primary parasites in the British Mobility of hosts.-The mobility of fauna (Table 2). Eastop (1973) referring hosts may either dampen or promote the to aphids noted that the production of a evolutionary process towards speciation of distinctive gall is always associated with parasites. High mobility of host stages host-plant specificity. Members of the Cy- which are infected with parasites reduces nipidae (238 species) also form but isolation of parasite populations important radiation has not been so extensive; evi- in speciation of parasites, discussed under dently the opportunities for radiation have Concepts 1 and 3. Static hosts such as not been as fully exploited as by the gall plants, or hosts of low mobility reinforce flies. isolation of parasite populations. Plants Specialization in parasites on animals disperse as seeds, a stage usually not in- should be more highly developed than in fected by parasites (important exceptions parasites on plants. Although animals as a are fungi, seed wasps and seed weevils). group are chemically more similar than Similarly, insects tend to disperse as very plants, herbivores have a greater diversity early larval stages before parasites attack of places to live than plants, and strong (e.g. Choristoneura fumiferana, Morris, and diverse behavioral, phagocytic and im- 1963; Porthetria dispar, Leonard, 1970) or mune defenses against parasites. Thus, more commonly in the adult stage which is finding and living with hosts seems to de- relatively free from parasitic insects. The mand a greater number of adaptations per contrary situation exists among some mam- species for parasites of animals than for mals, birds and fish, which are relatively parasites of plants, and therefore a nar- large, highly mobile animals. Parasitized rower host range. Members of the largest animals disperse, gene flow between para- families in the British fauna are parasites site populations is high and rates of diver- of insects: the Ichneumonidae (1938 spe- gence and speciation are reduced. It is cies) and Braconidae (891 species) (Table among the students of parasites on these 2). groups that the concept of slow evolution Probably the degree to which species of host and parasite are coevolved and the of parasites, relative to that of their hosts, proportion of the genome devoted to co- seems to have originated. Jordan (1942) could not have been appreciated supported this view based on studies of without extensive breeding of plants for fleas (Siphonaptera) which are restricted parasite resistance. Flor (1971) and Day to birds and , as are the lice (1974) provided strong evidence from (Phthiraptera) studied by other supporters plant breeding experiments that there is a such as Metcalf (1929) and Hopkins gene-for-gene relationship between the (1949). 416 PETER W. PRICE

Concept 5. Types of speciation other than on Mount Shasta in California a host shift through geographic isolation are at of the fruit fly, Rhagoletis indifferens, least as important as allopatric from bitter cherry, Prunus emarginata, to speciation. introduced domestic cherry, P. avium, could occur only at about 5,000 feet during There are probably several routes by the last two weeks of July, whereas the fly which species can be formed (Kinsey, occurred from sea level to 9,000 feet and 1937; White, 1968, 1973; Scudder, 1974; from May to October. Bush, 1975b) and sympatric speciation is Hosts with different phenologies or one likely route (Stebbins, 1964; Grant, breeding cycles may effectively isolate 1966; Maynard Smith, 1966; Spieth, their parasites allochronically and may 1968; Dobzhansky, 1970; Thoday, 1972; play an important part in sympatric spe- Bush, 1975b). Ross (1962) emphasized ciation. Triggering of reproductiveactivity the importance of host shifts that isolate may be initiated by the host as in the rab- sympatric populations and Mayr (1963) bit and hare fleas (Rothschild, 1965; stated that host races of ani- phytophagous Rothschild and Ford, 1964, 1973), insects mals provide the only case where incipient parasitic on others (Salt, 1941; Lees, sympatric speciation seemed to be possible. 1955), and possibly among blood-feeding If host race formation can lead to specia- Mallophaga on birds (Foster, 1969). tion of plant parasites it can also be im- From the gene-for-gene hypothesis Day portant among animal parasites. Rapid (1974) predicted the number of host races evolutionary rates and such extensive adap- that a set of resistant varieties will select tive radiation as seen among parasites is for. With 19 genes for resistance in apple, not easily explained by allopatric specia- for example, each of which may have two tion over extended time periods. The large phenotypes, resistant or susceptible, there numbers of sibling species are equally hard would be 219or 524,288 races of a parasite to explain by this model. Bush (1975b) adapted to exploit fully the range of ap- concluded that host races of plant parasites ple varieties. This may seem an extreme evolved sympatrically and that these were number, but we have every reason to infer undoubtedly the progenitors of the many that a parasite must be closely attuned sibling species so often found to be sym- morphologically, physiologically and bio- patric on different hosts. chemically to the host, and, therefore, such Bush (1974, 1975a) suggested that the extensive race formation may be necessary establishment of new host races may re- and Once the races have differen- quire only minor alterations in the genome. realistic. in way subtle, ecological or tem- His basic model accounts for speciation in- tiated this poral isolation could easily promote the volving only two alleles at each of two loci; one locus controlling host selection and the independent differentiation of populations. other controlling survival in the host. One Since most parasites are small, usually allele at each locus carries these traits with narrow tolerances to environmental adapted to host species A and the other al- factors, they are susceptible to minor spa- leles enable the parasite to discover and tial or temporal change. When tolerances exploit host species B. If host species A are narrow slight differences between hab- and B have different phenologies, and the itats may cause isolation where parasites adapt to these differences, repro- may be only 100 meters apart. If reproduc- ductive isolation is reinforced. Bush tives or dispersing individuals live only a (1975a) provided several examples of this few days, a week's difference in phenology allochronic isolation involving host shifts may prevent gene flow between popula- which can occur only through "a narrow tions. Many more exist for para- window in space and time." For example, sitic species and it is in these intermediate EVOLUTIONARY BIOLOGY OF PARASITES 417 and changeable zones that Stebbins (1974) ployed to examine the variation inherent sees the cradle for rapid evolution. For in siblings and populations, and its effect such small, short-lived, precisely adapted on survivorship; the physiological toler- organisms as parasites, evolution will oper- ances of individuals and its variation, both ate in miniature: short times, small spaces, within and between population centers. Fi- but impressive results. nally, the influence of host shifts should be investigated by direct observation of nat- FURTHER STUDY ural examples, especially before speciation, and by experimental manipulation. An ex- The general patterns envisaged for para- perimental approach to the evolutionary sitic species include small, relatively homo- biology of parasites, inadequately used to zygous populations with little gene flow date, holds great promise for the further between populations, which results in many development of concepts on the ecology specialized races, rapid evolution and spe- and evolution of parasites. ciation without geographic isolation, and an abundanceof sibling species. Short gen- SUMMARY eration times, with large fluctuations in population sizes, and narrow environmental There are probably more species of para- tolerances contribute importantly to the site than all non-parasite species combined. evolutionary potential of parasitic species. In the British insect fauna only 3.9% are Thus many of the factors involved in de- estimated to be predators, whereas 35.1% fining the "kind of species" (Mayr, 1963, are parasitic on plants, and 3 7.0% are Table 14-1) a parasite is, or the sort of parasitic on animals. In a parasite food genetic system likely to be found in para- chain based on plants, trends are probably sites can be inferred. These generaliza- in the direction of i) smaller size, ii) tions, reached by using the inductive pro- shorter life cycles, iii) more specialized cess, need critical evaluation based on species (i.e., lower ranges of tolerance), more information on natural populations in iv) less predictable resources, v) greater order to test the generality of the concepts population fluctuations, vi) more patchily proposed here. Parasitic species are not pe- distributed hosts, vii) greater isolation be- culiar in having their genetic systems in- tween populations, viii) higher evolution- adequately understood (cf. Mayr, 1963; ary rates. Five concepts are generated to Wilson et al., 1975), and all aspects of the account for the extensive adaptive radia- biology of these organisms need further tions seen among parasitic taxa: 1) Para- investigation. Here aspects central to the sites are adapted to exploit small, dis- understanding of parasite evolutionary continuous environments. 2) Parasites biology are considered. represent the extreme in the exploitation of In sexually reproducingparasites popula- coarse-grainedenvironments. 3) Evolution- tion structure requires much attention. ary rates and speciation rates are high. What is the effective population size, the 4) Adaptive radiation is extensive and de- distance moved by the dispersal phase of pends upon, a) the diversity of hosts being parasites, the frequency of gene flow from exploited, b) the size of the host target, one population to another, the behavior of c) the evolutionary time available, d) the individuals which influence mating patterns selective pressure for coevolutionary modi- within and between populations? The ge- fication and e) the mobility of hosts. 5) netics of parasite species and races should Types of speciation other than through receive much more attention. A compara- geographic isolation are at least as impor- tive approachusing both sexually and asex- tant as . Areas of em- ually reproducing parasites should be em- phasis for further study are discussed. 418 PETER W. PRICE

ACKNOWLEDGMENTS sects. Australia and New Zealand Book Co., Sidney. I am grateful to Guy Bush, Beverly . 1975a. Sympatric speciation in phytoph- Rathcke and John Thompson for reviewing agous parasitic insects. p. 187-206. In P. W. the manuscript and to William Heed, Price (ed.). Evolutionary strategies of para- Michael sitic insects and mites. Plenum, New York. Johnson, Marjorie Hoy and the . 1975b. Modes of animal speciation. An- Hon. Miriam Rothschild for making addi- nu. Rev. Ecol. Syst. 6:339-364. tional valuable suggestions or corrections. CARSON, H. L. 1968. The population flush and The beginnings of this paper were devel- its genetic consequences. p. 123-137. In R. C. oped at a symposium on the evolutionary Lewontin (ed.). Population biology and evo- of lution. Syracuse Univ. Press, Syracuse, New strategies parasitic insects and I owe York. much to the participants: Richard Askew, . 1975. The genetics of speciation at the Guy Bush, Don Force, Daniel Janzen, diploid level. Amer. Natur. 109:83-92. Robert Matthews, Rodger Mitchell and CHENG, T. C. 1973. General parasitology. Aca- Bradleigh Vinson. The National Institutes demic Press, New York. 965 p. of Health provided financial support CLAY, T. 1950. The Mallophaga as an aid to the classification of birds with special refer- through U.S. Public Health Training Grant ence to the structure of feathers. Proc. 10th PH GM 1076. Int. Ornith. Congr. p. 207-215. COLINVAUX, P. A. 1973. Introduction to ecol- LITERATURECITED ogy. Wiley, New York. 621 p. DARWIN, C. 1872. The origin of species. 6th ed. ANDREWARTHA,H. G., AND L. C. BIRCH. 1954. Murray, London. The distribution and abundance of animals. DARLINGTON, A. 1974. The galls of oak. 298- Univ. Chicago Press, Chicago. 782 p. 311. In M. G. Morris and F. H. Perring ARNDT, W. 1940. Der prozentuelle Anteil der (eds.). The British Oak. Classey, Faringdon, Parasiten auf und in Tieren im Rahmen des Berks. aus Deutschland bisher bekannten Tierarten- DAY, P. R. 1974. Genetics of host-parasite in- bestandes. Z. Parasitenkd. 11:684-689. teraction. Freeman, San Francisco. 238 p. ASKEW, R. R. 1968. Considerations on specia- DOBZHANSKY, T. 1970. Genetics of the evolu- tion in Chalcidoidea (Hymenoptera). Evolu- tionary process. Columbia Univ. Press. New tion 22:642-645. York. 505 p. . 1971. Parasitic insects. Elsevier, New DOGIEL, V. A. 1964. General parasitology. York. 316 pp. Oliver and Boyd, Edinburgh. 516 p. . 1975. The organization of chalcid-dom- DRITSCHILO, W., H. CORNELL, D. NAFUS AND B. inated communities centred upon O'CONNOR. 1975. : Of endophytic hosts. p. 130-153. In P. W. Price mice and mites. Science 190:467-469. (ed.). Evolutionary strategies of parasitic in- EASTOP, V. F. 1973. Deductions from the pres- sects and mites. Plenum, New York. ent day host plants of aphids and related in- sects. p. 157-178. In H. F. van Emden (ed.). ATSATT, P. R. 1973. Parasitic flowering plants: Ento- How did they evolve? Amer. Natur. 107:502- Insect/Plant relationships. Symp. Roy. 510. mol. Soc. London. 6. EHRLICH, P. R., AND P. H. RAVEN. 1964. But- BARNES, H. F. 1951. Gall midges of economic terflies and plants: A study in coevolution. importance. Vol. 5. Gall midges on trees. Evolution 18:586-608. Crosby Lockwood, London 270 p. EICHLER, W. 1948. Some rules in ectoparasitism. 1955. Gall midges reared from acorns and Ann. Mag. Natur. Hist. Ser. 12, 1:588-598. acorn cups. Entomol. Mon. Mag. 91:86-87. ELTON, C. S. 1927. Animal Ecology. Sidgwick with BROWN, W. J. 1959. Taxonomic problems and Jackson, London. 207 p. closely related species. Annu. Rev. Entomol. EMBREE, D. G. 1971. Operophtera brumata 4: 77-98. (L.), winter moth (Lepidoptera: Geometri- BRUES, C. T. 1924. The specificity of food dae). p. 167-175. In Biological control pro- plants in the evolution of phytophagous in- grammes against insects and weeds in Canada sects. Amer. Natur. 58:127-144. 1959-1968. Commonwealth Inst. Biol. Con- BUSH, G. L. 1974. The mechanism of sympatric trol. Tech. Comm. 4. host race formation in the true fruit flies FERNALD, M. L. 1950. Gray's manual of botany. (Tephritidae). p. 3-23. In M. J. D. White 8th ed. American Book Co., New York. 1632 (ed.). Genetic mechanisms of speciation in in- P. EVOLUTIONARY BIOLOGY OF PARASITES 419

FLOR, H. H. 1971. Current status of the gene- KENNEDY, C. R. 1975. Ecological animal para- for-gene concept. Annu. Rev. Phytopathol. 9: sitology. Blackwell, Oxford. 163 p. 2 75-2 96. KINSEY, A. C. 1937. An evolutionary analysis FORD, L. T. 1949. A guide to the smaller British of insular and continental species. Proc. Nat. Lepidoptera. South London Entomol. Natur. Acad. Sci. 23:5-11. Hist. Soc. London. 230 p. KLOET, G. S., AND W. D. HINCKS. 1945. A check FOSTER, M. S. 1969. Synchronized life cycles in list of British insects. Kloet and Hincks, Stock- the orange-crowned warbler and its malloph- port. 483 p. agan parasites. Ecology 50:315-323. KLUN, J. A., 0. L. CHAPMAN, K. C. MATTES, GRANT, V. 1966. The selective origin of incom- P. W. WoJTKowsKI, M. BEROZA AND P. E. patibility barriers in the plant genus Gilia. SONNET. 1973. Insect pheromones: Minor Amer. Natur. 100:99-118. amount of opposite geometrical isomer critical HARRISON, L. 1914. The Mallophaga as a pos- to attraction. Science 181:661-663. sible clue to phylogeny. Austr. Zool. 1: KREBS, C. J. 1972. Ecology. The experimental 7-11. analysis of distribution and abundance. Harper HEGNAUER, R. 1971. Chemical patterns and re- and Row, New York. 694 p. lationships of Umbelliferae. p. 267-277. In KuIJT, J. 1969. The biology of parasitic flower- V. H. Heywood (ed.). The biology and chem- ing plants. Univ. California Press, Berkeley. istry of the Umbelliferae. Academic Press, 246 p. London. LEES, A. D. 1955. The physiology of HEGNER, R. 1927. Host-parasite relations be- in . Cambridge Univ. Press, Lon- tween man and his intestinal protozoa. Cen- don. 151 p. tury, New York. 231 p. LEONARD, D. E. 1970. Intrinsic factors causing HERING, E. M. 1951. Biology of the leafminers. qualitative changes in populations of Porthetria Junk, The Hague, Netherlands. 420 p. dispar (Lepidoptera: Lymantriidae). Can. En- . 1957. Bestimmungstabellen der Blatt- tomol. 102:239-249. minen von Europa (einschliesslich des Mittel- LEVINS, R. 1962. Theory of fitness in a heter- meerbeckens und der Kanarischen Inseln). ogeneous environment. I. The fitness set and Junk, The Hague, Netherlands. Vols. 1-3. adaptive function. Amer. Natur. 96:361-373. 1185 p. + 221 p. LINDQUIST, E. E. 1969. Review of holarctic HEYWOOD, V. H. 1971. Systematic survey of tarsonemid mites (Acarina: ) par- Old World Umbelliferae. p. 31-41. In V. H. asitizing eggs of ipine bark beetles. Mem. En- Heywood, (ed.). The biology and chemistry tomol. Soc. Can. 60:1-111. of the Umbelliferae. Academic Press, London. MAcARTHUR, R. H., AND R. LEVINS. 1964. Com- HOPKINS, G. H. E. 1942. The Mallophaga as an petition, habitat selection and character dis- aid to the classification of birds. Ibis 14:94- placement in a patchy environment. Proc. 106. Nat. Acad. Sci. 51:1207-12 10. HOPKINS, G. H. E. 1949. The host-associations MAcARTHUR, R. H., AND E. 0. WILSON. 1967. of the lice of mammals. Proc. Zool. Soc. Lon- The theory of island biogeography. Princeton don 119:387-604. Univ. Press, Princeton, N.J. 203 p. JANZEN, D. H. 1968. Host plants as islands in MAYNARD SMITH, J. 1966. Sympatric speciation. evolutionary and contemporary time. Amer. Amer. Natur. 100:637-650. Natur. 102:592-595. MAYR, E. 1963. Animal species and evolution. - . 1973. Host plants as islands. II. Compe- Belknap Press of Harvard Univ. Press, Cam- tition in evolutionary and contemporary time. bridge, Mass. 797 p. Amer. Natur. 107:786-790. MAYR, E., E. G. LINSLEY, AND R. L. USINGER. . 1975. Interactions of seeds and their in- 1953. Methods and principles of systematic sect predators/parasitoids in a tropical decid- zoology. McGraw-Hill, New York. 328 p. uous forest. p. 154-186. In P. W. Price (ed.). METCALF, M. M. 1929. Parasites and the aid Evolutionary strategies of parasitic insects and they give in problems in , geographi- mites. Plenum, New York. cal distribution and paleogeography. Smith- JONES, A. W. 1967. Introduction to parasitol- sonian Misc. Coll. 81(8):1-36. ogy. Addison-Wesley, Reading, Mass. 458 p. MITCHELL, R. 1970. An analysis of dispersal in JORDAN, K. 1942. On Parapsyllus and some mites. Amer. Natur. 104:425-431. closely related genera of Siphonaptera. Rev. MORRIS, M. G. 1974. Oak as a habitat for in- Esp. Ent. 18:7-29. sect life. p. 274-297. In M. G. Morris and KELLOGG, V. L. 1913. Distribution and species- F. H. Perring (eds.). The British Oak. Clas- forming of ecto-parasites. Amer. Natur. 47: sey, Faringdon, Berks. 129-158. MORRIS, R. F. (ed.). 1963. The dynamics of 420 PETER W. PRICE

epidemic spruce budworm populations. Mem. lation in phytophagous insect communities: Entomol. Soc. Can. 31. 332 p. The pests of Cacao. Science 185:1064-1066. NOBLE, E. R., AND G. A. NOBLE. 1971. Para- STRONG, D. R., JR., AND D. A. LEVIN. 1975. sitology. The biology of animal parasites. 3rd of the parasitic fungi of Brit- ed. Lea and Febiger, Philadelphia. 617 p. ish trees. Proc. Nat. Acad. Sci. USA 72:2116- ODUM, E. P. 1971. Fundamentals of ecology. 2119. 3rd ed. Saunders, Philadelphia. 574 p. SUOMALAINEN,E. 1962. Significance of parthe- OLIVER, J. K., JR. 1971. Parthenogenesis in nogenesis in the evolution of insects. Annu. mites and ticks (Arachnida: ). Amer. Rev. Entomol. 7:349-366. Zool. 11:283-299. THODAY, J. M. 1972. Disruptive selection. OPLER, P. A. 1974. Oaks as evolutionary islands Proc. Royal Soc. London. Ser. B. 182:109-143. for leaf-mining insects. Amer. Sci. 62:67-73. THORPE, W. H. 1930. Biological races in insects ROELOFS, W. L., R. T. CARDE, R. J. BARTELL, AND and allied groups. Biol. Rev. 5:177-212. P. G. TIERNEY. 1972. attractant trap- TOMLINSON, J. 1966. The advantages of her- ping of the European corn borer in New York. maphrodism and pathenogenesis. J. Theoret. Environ. Entomol. 1:606-608. Biol. 11: 54-58. Ross, H. H. 1962. A synthesis of evolutionary TOWNES, H. 1969. The genera of Ichneumoni- theory. Prentice-Hall, Englewood Cliffs, N.J. dae. Part 1. Mem. Amer. Entomol. Inst. 11: 387 p. 1-300. ROTHSCHILD, M. 1965. The rabbit and hor- VINSON, S. B. 1975. Biochemical coevolution mones. Endeavour 24:162-168. between parasitoids and their hosts. p. 14-48. ROTHSCHILD, M., AND T. CLAY. 1952. Fleas, In P. W. Price (ed.). Evolutionary strategies flukes and . A study of bird parasites. of parasitic insects and mites. Plenum, New Collins, London. 305 p. York. ROTHSCHILD, M., AND B. FORD. 1964. Matura- WHITE, M. J. D. 1968. Models of speciation. tion and -laying of the rabbit flea (Spilop- Science 159:1065-1070. syllus cuniculi Dale) induced by the external . 1970. Heterozygosity and genetic poly- application of hydrocortisone. Nature 203: morphism in parthenogenetic animals. p. 237- 210-211. 262. In M. K. Hecht, and W. C. Steere (eds.). . 1973. Factors influencing the breeding of Essays in evolution and genetics in honor of the rabbit flea (): A Theodosius Dobzhansky. Appleton-Century- spring-time accelerator and a kairomone in Crofts, New York. nesting rabbit urine with notes on Cediopsylla -. 1973. Animal cytology and evolution. 3rd simplex, another "hormone bound" species. J. ed. Cambridge Univ. Press, London. 961 p. Zool. Lond. 170:87-137. WHITTAKER, R. H., AND P. P. FEENY. 1971. Al- SALT,G. 1941. The effects of hosts upon their lelochemics: Chemical interactions between insect parasites. Biol. Rev. 16:239-264. species. Science 171:757-770. SCUDDER,G. G. E. 1974. Species concepts and WILLIAMS, G. C. 1975. Sex and evolution. speciation. Can. J. Zool. 52:1121-1134. Princeton Univ. Press, Princeton, N.J. 200 p. SOUTHWOOD, T. R. E. 1961. The number of WILSON, A. C., G. L. BUSH, S. M. CASE, AND species of insect associated with various trees. M. C. KING. 1975. Social structuring of J. Anim. Ecol. 30:1-8. mammalian populations and rate of chromo- SPENCER, K. A. 1969. The agromyzidae of Can- somal evolution. Proc. Nat. Acad. Sci. 72: ada and Alaska. Mem. Entomol. Soc. Can. 5061-5065. 64:1-311. WRIGHT,S. 1940. Breeding structure of popula- SPIETH,H. T. 1968. Evolutionary implications tions in relation to evolution. Amer. Natur. of sexual behavior in . Evol. Biol. 74:232-248. 2:157-193. . 1943. Isolation by distance. Genetics 28: STEBBINS,G. L. 1964. The evolution of animal 114-138. species. Evolution 18: 134-137. . 1949. Adaptation and selection. p. 365- . 1974. Flowering plants. Evolution above 389. In G. L. Jepsen, E. Mayr, and G. G. the species level. Belknap Press of Harvard Simpson (eds.). Genetics, paleontology, and Univ. Press, Cambridge, Mass. 399 p. evolution. Princeton Univ. Press, Princeton, STRONG, D. R., JR. 1974a. The insects of British N.J. trees: equilibration in ecological ZIMMERMAN, E. C. 1960. Possible evidence of time. Ann. Missouri Bot. Gard. 61:692-701. rapid evolution in Hawaiian moths. Evolu- 1974b. Rapid asymptotic species accumu- tion 14: 137-138.