Vernon Kellogg, Host-Switching, and Cospeciation - BioOne

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these concepts (Klassen, 1992; Brooks and McLennan, 1993; Hoberg et al., 1997) credit the origin of one or both of these concepts to Vernon. Lyman Kellogg ...
CRITICAL COMMENT . . . J. Parasitol., 88(5), 2002, pp. 1045–1048 ! American Society of Parasitologists 2002

Vernon Kellogg, Host-Switching, and Cospeciation: Rescuing Straggled Ideas Anindo Choudhury, Brian R. Moore*, and Fernando L. P. Marques†, Division of Natural Sciences, St. Norbert College, 100 Grant Street, De Pere, Wisconsin 54115. e-mail: [email protected] Cospeciation and host-switching have become central concepts in host–parasite coevolutionary studies (Brooks, 1981; Hafner and Nadler, 1988, 1990; Brooks and McLennan, 1993; Page, 1993, 1994). Parasite speciation may either be concomitant with and resulting from host speciation (cospeciation) or follow the colonization of a ‘‘new’’ host from an existing one (host-switching). Historical summaries that deal with these concepts (Klassen, 1992; Brooks and McLennan, 1993; Hoberg et al., 1997) credit the origin of one or both of these concepts to Vernon Lyman Kellogg, an entomologist at Stanford, who specialized on the taxonomy and distribution of the mallophagan lice of birds and mammals. The issue is not without its intrigue and controversy however; another leading mallophagan systematist of the time, Wolfdietrich Eichler (Eichler, 1942, 1948), apparently accused Kellogg of ‘‘stealing’’ the idea of cospeciation from Fahrenholz (Klassen, 1992). According to Klassen (1992), the issue is settled in favor of Kellogg because he had the idea before Fahrenholz did. During the course of research on the logic and implications of the host–parasite method in biogeography, see Marques (2000), for example, it was discovered that Kellogg did not ascribe any evolutionary significance to ‘straggling,’ nor did he address cospeciation until he became aware of Fahrenholz’s work. The present critical comment discusses these conclusions. In supporting our contentions, Kellogg’s own writings have been quoted extensively because this approach leaves little room for misinterpretation and allows the readers to judge for themselves the validity of the conclusions reached here. Kellogg’s ‘‘straggling’’ and evolutionary host-switching: It is commonly believed that the phenomenon of host-switching was described and discussed at length by Kellogg, as ‘‘straggling,’’ in works dealing with the Mallophaga of birds and mammals (Kellogg, 1896a, 1986b, 1913a, 1914; Kellogg and Kuwana, 1902). It appears that Kellogg first used the word ‘‘straggling’’ in 1896 (Kellogg, 1896a) to explain the presence of a mallophagan species on an ‘‘unexpected host’’ (by this, Kellogg meant a host that was distantly related and, therefore, not expected to have the parasite). This presence was caused either by migration in situations where distantly related birds come in close contact (as in roosting maritime birds) or by ‘‘straggling after death of the host’’ as in the case when ‘‘contact could occur between birds of prey and their victims’’ (Kellogg, 1896a). Later, in the same monograph, Kellogg (1896a) discusses the conditions under which mallophagans were often collected for taxonomic studies and cautions against the practice of collecting these ectoparasites from dried skins in museum collections: ‘‘There is also much likelihood of ‘straggling’ and little opportunity to prove or disprove it’’ and goes on to recommend the following. ‘‘It is evident, in face of the fact that after death of host, many parasites leave the body, that much care must be taken to prevent ‘straggling,’ i.e., parasites from one bird getting upon some other bird which may be conveniently near’’ (Kellogg, 1896a). This clearly shows that Kellogg, at least in 1896, was not using the term ‘‘straggling’’ to describe anything more than accidental occurrences. The next mention of straggling is made in 1902, when Kellogg and Kuwana (1902) attempted to use the mallophagans to elucidate the host relationships between the birds of the Galapagos and their mainland South American relatives (Kellogg and Kuwana, 1902). However, they noted that ‘‘an extraordinary condition, . . . attending the distribution of the parasites among birds of the islands, made such an attempt even less profitable than it might otherwise have been (Kellogg and Kuwana, 1902).’’ * Department of Ecology and Evolutionary Biology, Yale University, 165 Prospect Street, New Haven, Connecticut 06520-8106. † Universidade Estadual Paulista, IBB—Departamento de Zoologia, Botucatu, Sa˜o Paulo, Brazil.

Their experience is best described in their own words (emphasis ours): When the authors first began the examination of these Mallophaga, they were startled by the unusual eccentricity of the occurrence of the parasite on the various bird hosts. A species of Mallophaga, obviously normal in such a strictly land bird as Geospiza would be found to occur occasionally on such strictly maritime birds as terns and The first cases of this kind met with in working over the collection were attributed to mistakes in the collectors records, or to straggling after death when the birds’ bodies were in occasional contact in the game bag or on the skinning table. Kellogg and Kuwana (1902) soon realized that the records were bonafide and that they had ‘‘to do with an abnormal phase of normal straggling.’’ They explained that this unique condition of ‘‘abundant parasitism, is, of course, also caused by the unusual facility of migration (or normal straggling) afforded by the forced gregarious habits of the islands’ birds.’’ Kellogg returns to the subject of straggling in 1913 (Kellogg, 1913a), this time from prey to predator during feeding. He feels it ‘‘indeed important to note that no mammal-infesting Mallophaga have been taken from any vulture, despite the excellent chances of such straggling’’ and speculates that differences in the physiologies of the hosts or the adaptive specializations (or both) of the parasites do not permit straggling. Kellogg goes on to point out that the few records of distantly related species of mallophagans on raptors are ‘‘plainly stragglers from prey’’ (Kellogg, 1913a). Similarly, Kellogg’s explanations for exceptional records of the same species of parasite on distantly related mammalian hosts (Kellogg, 1914) also clearly indicate that, as in 1896, he considered straggling to be the cause of accidental or incidental occurrences. Apart from the usage itself, it is also noteworthy that Kellogg’s ‘‘straggling’’ involves the same species of parasite in often distantly related hosts be it accidental and temporary, or more natural (as in the case of the Galapagos birds). This phenomenon makes no predictions about the evolutionary fate, e.g., speciation, of the straggler. Kellogg’s straggling is in fact host-sharing, or broad coaccommodation (Brooks, 1979). This is also observed in many endohelminths, where a parasite species often has a typical host but is occasionally found in other, often atypical, hosts because of overlap in habit and habitat of the hosts (similar ecologies) or common host-physiological conditions required by the parasite, etc. Straggling cannot, and should not, be equated with hostswitching; doing so reduces the status of host-switching from an evolutionary phenomenon to a description of all incidental infections. Brooks and McLennan (1993) provide several examples of ‘hostswitching’ without speciation, albeit within the context of phylogenetic analyses. However, if host-switching is itself simply host-sharing, then there is no need for a phylogenetic analysis to reveal this pattern or how common it is; a simple enumeration of hosts from a survey would indeed be sufficient. For instance, Crepidostomum cooperi Hopkins, 1934, is a fish parasite with a long host list. It is commonly found in hosts (e.g., Perca flavescens, Lepomis spp., Percopsis omiscomaycus etc.) that often occur sympatrically and belong to several distantly related families (Percidae, Centrarchidae, and Percopsidae respectively), (Margolis and Arthur, 1979; McDonald and Margolis, 1995; Hoffman, 1999, and references therein). If we regard this as an example of hostswitching, a phylogenetic analysis may reveal the ‘‘donor’’ and ‘‘recipient’’ hosts, i.e., the direction in which such a host-switch (without speciation) took place, but an analysis is not necessary in order to state that host-switching is common in this trematode. Indeed, a perusal of host-lists for species of freshwater fish parasites (Margolis and Arthur, 1979; McDonald and Margolis, 1995; Hoffman, 1999) reveals that many endoparasites have been reported from several distantly related

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hosts. Taxonomic problems and misidentifications notwithstanding, there does seem to be considerable natural straggling (host-sharing) in many species of parasites, but can we call these host-switching events without confusing the issue completely? A distinction between these 2 phenomena (host-sharing or broad coaccommodation, and host-switching as a speciation mode) has been recognized in the past. Chabaud (1965) distinguished between ‘‘transfuge’’ (French ! spillover) which is equivalent to Kellogg’s straggling, and ‘‘capture’’ which involves a speciation event (see Xie et al., 1994; Combes, 2001). Host-switching is a 2-step process involving natural straggling (acquisition of new hosts in contemporary ecological time) as envisioned by Kellogg, but also speciation in the ‘‘newly’’ acquired host. Viewing Kellogg’s straggling or host-sharing as hostswitching confuses these 2 distinct phenomena (e.g., Patterson et al., 1993; Ro`sza, 1993). The term ‘‘host-transfer’’ (Combes, 2001) finds itself in a similar situation because a clear distinction between hostsharing and ‘‘transfer-speciation’’ has obviously not been made (a problem recognized by Combes, 2001, p. 173). Numerous examples of hostswitching (involving distinct species, not straggling) in animal parasites have been hypothesized and discussed quite some time back by various authors (e.g., Bykhovsky, 1957; Michailov, 1962; Dogiel, 1964; Chabaud, 1965; Rysavy, 1968; Gusev, 1978; Price, 1980, etc.). It has also been extensively discussed in more recent literature (see Brooks and McLennan, 1993, and references therein). A similar phenomenon of speciation by ‘‘host-shifting’’ in plant-parasitic insects (Bush, 1975; Price, 1980) has been, and continues to be, the subject of intensive investigation (Bush, 1969; Feder, 1998; Johnson and Gullberg, 1998, other studies in Howard and Berlocher, 1998). The idea of speciation by host-shift, however, appears to have had independent roots in the botanical literature (Walsh, 1864, referenced in Howard and Berlocher, 1998). How then did Kellogg’s straggling come to be equated with (evolutionary) host-switching? A chronological perusal of the literature on the subject reveals that the (inadvertent?) switch was made by Launcelot Harrison (Harrison, 1914), an Australian mallophagan systematist, who elevated Kellogg’s concept of ‘‘straggling’’ to an evolutionary level (a careful reading of Von Ihering [1902] suggests that he was also discussing the same phenomenon). For Harrison, the challenge came from the mallophagan lice on Australian marsupials, exclusively comprising species belonging to the Boopidae, which were morphologically similar, and hence regarded by Harrison to be ‘‘closely related to the lowest and most generalized bird-frequenting genus, Menopon.’’ Harrison concluded: ‘‘It seems more reasonable to me to suppose that the migration upon marsupials was of ancient rather than recent occurrence’’ (Harrison, 1914, p. 9) and again toward the end of his paper (emphasis ours): And there is also the straggling difficulty. The genus Laemobothrium is found upon diurnal Accipitres, and upon a number of waterfowl which in ordinary course might form the food of the larger hawks. The position of the Accipitres is entirely unknown. Possibly there is a phyletic connection between them and the waterfowl. Equally possibly, the genus Laemobothrium may have straggled from one to the other, when some primitive hawk was engaged in devouring a primitive waterfowl (Harrison, 1914). It is uncertain whether the term host-switching (Brooks, 1981; Brooks and Glen, 1982) was borrowed or coined de novo; what is clear however is that as an evolutionary concept, it can no longer be attributed to Vernon Kellogg. Vernon Kellogg and cospeciation: From the very beginning and throughout his work, Kellogg emphasized the presence of the same species of parasite on closely related, but geographically widely separated, hosts (see also discussion by Metcalf, 1929; Dogiel, 1964). As early as 1896, Kellogg (1896a) set the tone of what was to become the central thesis of his life’s work (emphasis ours): With the spreading of the ancestral bird-species, geographical races have arisen within the limits of the species, which have, with time and isolation caused by newly appearing geographical barriers (caused by geologic or climatic changes), come to be distinct species—species often distinguished only by superficial differences in color, etc. The parasites have remained practically unaffected by the conditions which have produced the differences among the birds; the temperature of the host’s body, the feathers as food, all of the environment is essentially unchanged in its relation to the

parasite. The parasite species thus remains unchanged, while the first Larus species or Anas species becomes differentiated into a dozen or score of specific forms, all with a common parasite. This idea was repeated in 1905 and again in 1907 (Kellogg, 1905, 1907). In his 1913 paper on the ‘‘distribution and species forming of ecto-parasites,’’ Kellogg (1913a) concludes by summarizing the nature and evolution of mallophagan host-associations (emphasis ours): First, there is apparent in Mallophagan distribution a general faithfulness of parasite to host kind or groups of related host-kinds, and this without much reference to geographical conditions. And second, there appears to be a plain tendency for a single parasite species to be common in two or more related host species, even though these hosts be so widely separated geographically and so restricted in their separate geographical ranges that all possible chance of contact between individuals of the different host species seem positively precluded. Kellogg saw ‘‘but one answer’’ to this actual condition, that is, that the parasite species has been handed down practically unchanged to the present specifically and even generically distinct several bird species from their common ancestor of earlier days. The parasite species dates from the days of this ancestor. A slightly modified version appears in his 1914 paper on the mallophagans of mammals, where Kellogg states that closely related host species have the same or closely related parasites. As an explanation, Kellogg (1914) repeated his thesis that ‘‘the common parasite species has persisted unchanged from a common ancestor of the now divergent but allied host kinds.’’ Although this explains the presence of the same species of parasite on related hosts, curiously enough it does not address cospeciation. In fact, the addition of the phrase ‘‘or closely related parasites’’ as a caveat to his often-repeated observation that related but widely separated host species have the same species of parasite appears late and apparently just this once in his writings (Kellogg, 1914). It becomes clear that what Kellogg was discussing at length was not cospeciation but rather the lack of it. Kellogg was a pioneer and champion of the idea that parasite speciation lags behind host speciation, the so-called ‘‘Manter’s first rule’’ (Brooks and McLennan, 1993), which should be more appropriately named ‘‘Kellogg’s rule.’’ In contrast to Kellogg’s writings, Fahrenholz’s (1913) thesis is as explicit a statement of cospeciation as one can expect. Using evidence from the ectoparasitic anoplurans (sucking lice) of primates, he concludes Since the parasites as living beings are dependent on their living conditions (habitat, environment) . . . therefore, generally, one will find on hosts of the same species, parasites of the same species and on hosts of different species, the parasites will diverge from one another to the same degree that their hosts are related’’ (translation from the German after Klassen, 1992). The first clear discussion of ‘‘cospeciation’’ (parallel lineage splitting) by Kellogg was in a paper largely devoted to discussing this work by Fahrenholz (1913). Kellogg’s paper (Kellogg, 1913b) seems to have been aimed at providing an English version synopsis of Fahrenholz’s findings (see title of Kellogg’s 1913b paper) and relating them to his own views on speciation in the mallophagans (biting lice). Although he considers Fahrenholz’s findings supportive of his own views, Kellogg is, in the end, largely unsuccessful in dovetailing Fahrenholz’s idea of parallel lineage splitting of host and parasite with his own often-repeated thesis that host speciation has not been accompanied by parasite speciation. As to Fahrenholz’s observations upholding Kellogg’s ideas, it is true insofar as the relationships of the host determine the host associations (and specificity) of the parasite and the parasites can be used to provide insight into host relationships. Incidentally, the potential of parasites to reveal host relationships was discussed earlier, by pioneer fish parasitologist, Edwin Linton (Linton, 1894). Unfortunately, the idea that parasites can provide insights into the relationships of their hosts may be mistaken as evidence of Kellogg’s belief in cospeciation. Without intending to ascribe motives, it may be noted that it is nevertheless intriguing that Kellogg qualified his earlier stance on the lack of parasite speciation in the face of host speciation by adding the words ‘‘or closely related’’ in his very next paper in 1914, after having read and written about Fahrenholz’s work! No wonder then if Eichler was adamant that

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the concept be credited to Fahrenholz. It would appear that, invective and style notwithstanding, Eichler was on the right side of the facts. It is also intriguing that Kellogg, while having a masterful grasp of the major so-called nonDarwinian theories of species forming, e.g., geographic isolation (Wagner [1868] in Kellogg, 1907), in free-living organisms (see Kellogg, 1907; Jordan and Kellogg, 1907), did not extend the same argument to the parasites he was studying. A closer examination of Kellogg’s writings reveals why. According to Kellogg, the two ‘‘influences resulting from the peculiar habits of the Mallophaga,’’ i.e., lack of speciation in the face of host speciation and the fixing of small local variations caused by isolation (of groups of individuals) had important results, which manifest to any student of the group, are to render difficult the division of the order into distinct genera on account of the general similarity of structure, and to make difficult the definition of species on account of the many slight variations among the individuals from different bird individuals. Later, in the same paper, Kellogg (1896a) says: Although the Mallophaga include already nearly 1,000 described species, there are but few genera and these genera are difficult to separate. In other words, the whole group is a series of closely related and intergrading forms. Kellogg believed that without any drastic change of habitat, or infestation heavy enough on any one bird to cause competition among the lice, the resulting lack of any particular selection pressure would inevitably lead to the origin of small variations purely caused by isolation on individual lineages of birds, particularly on solitary bird species but within the limits of species boundaries (see also, Kellogg, 1907). Not only was Kellogg one of the foremost champions of evolution in North America at the turn of the 20th century (Gould, 1998) but his writings (Kellogg, 1907, 1924) also reveal his strong advocacy of natural selection over geographic isolation (cf. Jordan [1905] quoted in Kellogg, 1907). He held that geographic isolation ‘‘is a tremendously favouring condition but not a primary cause of species-forming’’ (Kellogg, 1907) and that natural selection was the ‘‘final arbiter’’ in the production of new species. ‘‘Geographic isolation’’ is discussed, along with several others, under the common heading of ‘‘other theories’’ or ‘‘auxiliary theories’’ of species forming (Kellogg, 1907; chapter IX). Kellogg’s views on the very nature of mallophagan species, their host-relationships, and variation led him away from cospeciation, to emphasize the lack of it, even though, in some cases, he appeared to have the evidence for it: While I believe myself able to refer specimens taken from American birds to a score of species described from specimens taken from European and Asiatic birds, in all of these instances there are slight but recognizable differences between the American specimens and the type-forms of the species . . . (Kellogg, 1896a). There were also cases where it would appear that the evidence stared him in the face. For example, in his report of D. pertusus Nitzsch, from the American coot Fulica americana, Kellogg noted disagreement in one morphological feature between North American specimens and those from the European coot Fulica atra but did not ascribe any real significance to it. In his review of Fahrenholz’s work (Kellogg, 1913b), Kellogg stated that he did not have the raw material that would allow him to make the case for cospeciation in mallophagans as Fahrenholz clearly did with the anopluran lice in primates. For the most part, a careful reading of his taxonomic accounts and decisions (Kellogg, 1896a, 1896b, 1899) indicates that this is true. The Vernon Kellogg story is one of what could have been, but was not—so close and yet so far. It illustrates how the theoretical views held today shape the perception and interpretation of historical facts. Perhaps the problem lies in assuming that Kellogg required cospeciation to reveal phylogenetic relationships of hosts and then turning that around: because Kellogg was using parasites to uncover host phylogenetic relationships, he must therefore have been advocating cospeciation. It must be concluded then that Vernon Kellogg, although bringing to our attention a phenomenon that has subsequently been recognized by scores of parasitologists (parasite speciation apparently lags behind host

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speciation), did not recognize cospeciation as a significant speciationmode in parasites until Fahrenholz laid it all out in 1913. A.C. wishes to acknowledge Thomas Czechmeister for help with translation of some of Eichler’s writings. Much of the early discussion of this subject matter took place at the Department of Zoology, University of Toronto, during our time in the laboratory of Dan Brooks. Francesco Santini’s moral support is appreciated. A.C. thanks Dan Brooks for reading an earlier draft of this manuscript and for discussions on Kellogg and Jordan. A.C. would like to acknowledge an NSERC postdoctoral fellowship at the University of Toronto with Dan Brooks. LITERATURE CITED BROOKS, D. R. 1979. Testing the context and extent of host-parasite coevolution. Systematic Zoology 28: 299–307. ———. 1981. Hennig’s parasitological method: A proposed solution. Systematic Zoology 30: 229–249. ———, AND D. R. GLEN. 1982. Pinworms and primates: A case study in coevolution. Proceedings of the Helminthological Society of Washington 49: 76–85. ———, AND D. A. MCLENNAN. 1993. Parascript. Parasites and the language of evolution. Smithsonian Institution Press, Washington, D.C., 429 p. BUSH, G. L. 1969. Sympatric host race formation and speciation in frugivorous flies of the genus Rhagoletis (Diptera: Tephritidae). Evolution 23: 237–251. ———. 1975. Modes of animal speciation. Annual Review of Ecology and Systematics 6: 339–364. BYKHOVSKY, B. E. 1957. Monogenetic trematodes. Their systematics and phylogeny. American Institute of Biological Sciences, Washington, D.C., 627 p. [English translation.] CHABAUD, A. G. 1965. Particularite´s physiologiques des ne´matodes: Spe´cificite´ parasitaire. In Traite´ de Zoologie, vol. 4, part 2, P.-P. Grasse´ (ed.). Masson, Paris, France, p. 548–557. COMBES, C. 2001. Parasitism. The ecology and evolution of intimate interactions. University of Chicago Press, Chicago, 728 p. [Translated from the French original, 1995, by Isaure de Buron and Vincent A. Connors.] DOGIEL, V. A. 1964. General parasitology. Oliver and Boyd, London, U.K., 516 p. [English Translation of 3rd ed.] EICHLER, W. 1942. Die Entfaltungsregel und andere Gesetzma¨ssigkeiten in den parasito-genetischen Beziehungen der Mallophagen und anderer sta¨ndinger Parasiten zu ihren Wirten. Zoologischer Anzeiger 137: 77–83. ———. 1948. Evolutionsfragen der Wirtsspezifitat. Biologisches Zentralblatt 67: 373–406. FAHRENHOLZ, H. 1913. Ectoparasiten und Abstammungslehre. Zoologischer Anzeiger 41: 371–374. FEDER, J. L. 1998. The apple maggot fly, Rhagoletis pomonella: Flies in the face of conventional wisdom about speciation. In Endless forms, species and speciation, D. J. Howard and S. H. Berlocher (eds.). Oxford University Press, Oxford, U.K., p. 130–144. GOULD, S. J. 1998. Rocks of ages. Science and religion in the fullness of life. Random House Publishing Inc., New York, 241 p. GUSEV, A.V. 1978. Monogenoidea of freshwater fishes: Principles of systematics, analysis of world fauna and its evolution. Parazitologicheskii Sbornik 28: 96–198. HAFNER, M. S., AND S. A. NADLER. 1988. Phylogenetic trees support the coevolution of parasites and their hosts. Nature 332: 258–259. ———, AND ———. 1990. Cospeciation in host–parasite assemblages: Comparative analysis of rates of evolution and timing of cospeciation events. Systematic Zoology 39: 192–204. HARRISON, L. 1914. The Mallophaga as a possible clue to bird phylogeny. Australian Zoologist 1: 7–11. HOBERG, E. P., D. R. BROOKS, AND D. SIEGEL-CAUSEY. 1997. Host-parasite co-speciation: History, principles, and prospects. In Host-parasite evolution: General principles and avian models, D. H. Clayton and J. Moore (eds.). Oxford University Press, Oxford, U.K., p. 212–235. HOFFMAN, G. L. 1999. Parasites of North American freshwater fishes, 2nd ed. Cornell University Press, Ithaca, New York, 539 p. HOWARD, D. J., AND S. H. BERLOCHER 1998. Endless forms, species and speciation. Oxford University Press, Oxford, U.K., 470 p.

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