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Evolution of the Schistosomes (Digenea: Schistosomatoidea): the Origin of Dioecy and Colonization of the Venous System

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Evolution of the Schistosomes (Digenea: Schistosomatoidea): the Origin of Dioecy and Colonization of the Venous System University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Faculty Publications from the Harold W. Manter Laboratory of Parasitology Parasitology, Harold W. Manter Laboratory of 12-1997 Evolution of the Schistosomes (Digenea: Schistosomatoidea): The Origin of Dioecy and Colonization of the Venous System Thomas R. Platt St. Mary's College Daniel R. Brooks University of Toronto, [email protected] Follow this and additional works at: https://digitalcommons.unl.edu/parasitologyfacpubs Part of the Parasitology Commons Platt, Thomas R. and Brooks, Daniel R., "Evolution of the Schistosomes (Digenea: Schistosomatoidea): The Origin of Dioecy and Colonization of the Venous System" (1997). Faculty Publications from the Harold W. Manter Laboratory of Parasitology. 229. https://digitalcommons.unl.edu/parasitologyfacpubs/229 This Article is brought to you for free and open access by the Parasitology, Harold W. Manter Laboratory of at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications from the Harold W. Manter Laboratory of Parasitology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. J. Parasitol., 83(6), 1997 p. 1035-1044 ? American Society of Parasitologists 1997 EVOLUTIONOF THE SCHISTOSOMES(DIGENEA: SCHISTOSOMATOIDEA): THE ORIGINOF DIOECYAND COLONIZATIONOF THE VENOUS SYSTEM Thomas R. Platt and Daniel R. Brookst Department of Biology, Saint Mary's College, Notre Dame, Indiana 46556 ABSTRACT: Trematodesof the family Schistosomatidaeare consideredvenous system specialists whose sister group is the vas- cular system generalists(Spirorchidae) of turtles. Colonizationof homeothermsby vasculartrematodes required precision egg laying near the conduit for egg passage to the external environmentand avoidance of pathogenesisthat might result in the prematuredeath of the host. Evolution of dioecy from the hermaphroditiccondition may have proceededthrough androdioecy in which hermaphroditeswere specializedfor precisionegg placementin the vascularsystem and largeradults became functional males. The evolutionof nucleargenes suppressingfemale functionalong with cytoplasmicgenes suppressingmale functioncould then have resulted in the origin of dioecious, dimorphicpopulations. Schistosomes compensated for the reductionin potential reproductivepartners by (1) increased overdispersionin the vertebratehost, (2) reduced egg hatching time in the external environment,(3) formationof permanentpairs mimickingthe hermaphroditiccondition, (4) increasedlongevity in the definitive host, and (5) increasedfecundity. Colonization of the venous system was necessitatedby (1) evolutionaryradiation into terrestrial vertebratesand (2) the increasedimmunopathology associated with the high, constantbody temperatureof homeothermicver- tebrates.The immune response to spirorchidand schistosome eggs appearsto be qualitativelysimilar in their respectivehosts. The arterialdwelling spirorchidsrelease eggs in the directionof blood flow, resultingin a wide disseminationof eggs within the host. The lower body temperatureof poikilothermsaccompanied by the seasonal natureof the immuneresponse in these hosts would result in a quantitativelyreduced pathogenesis. Hosts that did succumb to the infection would most likely die in water, where eggs could be released by predation,scavengers, or decompositionand develop successfully.Colonization of the venous system by schistosomeswould requireprecision egg placementbecause eggs are releasedagainst blood flow. Eggs are sequestered within the portal system of homeotherms,thus restrictingegg dispersal and resultingpathogenesis to less sensitive organs. A significantnumber of eggs may escape into the externalenvironment before a heavily infected host is incapacitatedby, or dies from, the infection. The schistosomes (Digenea: Schistosomatidae), because of SPIRORCHIDS AND SCHISTOSOMES their importance as human pathogens, are the most thoroughly The studied digenetic trematodes. Despite the enormous effort made Superfamily Schistosomatoidea contains 3 families: San- and to understand the immunology, biochemistry, genetic structure, guinicolidae (fish), Spirorchidae (turtles), Schistosomatidae (crocodilians, birds, and Life and and life history of these debilitating helminths, little effort has mammals). cycle morpholog- ical data identify these 3 families as a monophyletic taxon, with been made to elucidate, or even speculate on, the evolution of the spirorchids the sister-group of the schistosomatids (Brooks this fascinating group of organisms. This is regrettable, though et al., 1985, 1989). If the monoecious Spirorchidae is the sister- not surprising; as Brooks and McLennan (1993c) showed, little group of the dioecious Schistosomatidae, we should look to the of parasite evolutionary biology postdates the orthogenesis spirorchids for clues to the evolutionary history of the schis- movement of 1890-1940. The most puzzling aspect of schis- tosomes. tosome is the evolution of the dioecious condition from biology Species of the Schistosomatoidea share commonalities in life hermaphroditic ancestors. Of the more than 100 nominal fam- history and transmission patterns. All have brevifurcate furco- ilies of (> 10,000 species) digeneans described, only the Schis- cercous cercariae that develop to sexual maturity following di- tosomatidae (comprising approximately 100 species) are exclu- rect penetration of the definitive host (Yamaguti, 1975) and typ- sively gonochoristic. Combes (1991) termed the failure to ex- ically occupy the circulatory system as adults. Spirorchids may plain this evolutionary novelty a "scandal." be considered vascular system generalists with a preference for The advent of modem methods of phylogenetic analysis and the heart and arterial system of their chelonian hosts (Yamaguti historical ecology (Brooks and McLennan, 1991) has made it 1971, 1975). Spirorchids have also been reported regularly from possible to investigate major patterns of parasite evolution with- extravascular sites (Stunkard, 1923; Ulmer, 1959; Holliman et in a rigorous framework (Brooks and McLennan, 1993c). al., 1971; Brooks and Mayes, 1975; Brooks, 1979; Platt, 1993; Couching evolutionary hypotheses in explicit phylogenetic T. Platt, pers. obs.). Conversely, schistosomes are venous spe- terms has been shown to be an effective way to suggest exper- cialists with the exception of Dendritobilharzia pulverulenta, imental studies designed to elucidate the mechanisms respon- which inhabits the mesenteric arteries of ducks (Vande Vusse, sible for observed evolutionary patterns (e.g., McLennan, 1979). The 2 1996). This should be as true for parasites as for free-living major issues requiring explanation in schistosome evo- lution are the of and the species because parasites, as a group, do not appear to exhibit origins dioecy colonization of the ve- nous these events in a coherent scenario ne- any unique or distinctive pattern of evolutionary diversification system. Placing cessitates a examination of (Brooks and McLennan, 1993a, 1993b, 1993c). comparative reproductive strategies of spirorchids and schistosomes as well as the immunological response to these helminths by poikilothermic and homeotherm- ic hosts. Basch (1991) provided an extensive review of the mor- Received 26 February1997; revised 14 May 1997; accepted 14 May 1997. phology and reproductive biology of the schistosomes, and we * Departmentof Zoology, Universityof Toronto,Toronto, Ontario, Can- refer the interested reader to that source for the pertinent liter- ada M5S 1A1. ature in the ensuing discussion. 1035 1036 THEJOURNAL OF PARASITOLOGY,VOL. 83, NO. 6, DECEMBER1997 FROM HERMAPHRODITISMTO DIOECY 1995); however, intraspecific mate preferences are unknown (Read and Nee, 1990). The results presented by Nollen (1983) The development of dioecy in schistosomes has been asso- and Fried (1986) above suggest that hermaphroditic digeneans ciated with the origin of endothermy (Grossman et al., 1981; possess mate-finding abilities, so it is not surprising to find that Short, 1983), the development of the more sophisticated im- schistosomes also possess mate-finding capabilities. Whereas mune system present in endothermic vertebrates (Combes, genetic diversity may be necessary to maintain successful pop- 1991), or the shift from arterial to venous habitat accompanied ulations, it is not sufficient to explain the origins of dioecy by the development of the homeotherm portal system and sub- within the group. sequent colonization of terrestrial rather than primarily aquatic Why should schistosomes abandon the clearly successful her- hosts (Basch, 1991). Chromosomal inversion and translocation maphroditic life style? Dioecious parasitic platyhelminths are have been invoked to derive the heterogametic schistosome rare but occur among the Digenea, Monogenea, and Eucestoda karyotype from the homogametic karyotypes found in spiror- and inhabit gills, intestines, and circulatory systems. It would chids (Grossman et al., 1981; Short, 1983) although "presex" appear that this is a rare event that is not habitat specific, that chromosomes were reported in a small number of spirorchid is, becoming dioecious is not an adaptation to a particular hab- cell preparations (Grossman et al., 1981). Basch (1991) con- itat. Consequently, we should ask what is lost and what is cluded that the chromosomal changes accompanied, but did not gained by the organisms themselves? Three models have been cause, the transition from
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