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Sex Allocation and Population Structure in Apicomplexan

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Sex Allocation and Population Structure in Apicomplexan Sexallocationa ndpopulationst ructure inapicomplexan(protozoa)parasites Stuart A.West *,Todd G.Smithand AndrewF .Read Institute of Cell,Animal and Population Biology,University of Edinburgh, Edinburgh EH9 3JT,UK Establishingthe sel¢ng rate ofparasites isimportantfor studies inclinical and epidemiological medicine aswell as evolutionary biology .Sexallocation theory o¡ ers arelativelycheap and easy way to estimate sel¢ng rates innatural parasite populations. Local mate competition(LMC) theorypredicts that the optimalsex ratio ( r*;de¢ned as proportion males) is relatedto the sel¢ng rate ( s)bythe equation r* (17s)/2.In this paper,we generalize the applicationof sex allocation theory across parasitic protozoaˆ in the phylumApicomplexa. This cosmopolitan phylum consists entirelyof parasites, and includesa number ofspecies ofmedical and veterinary importance. W esuggestthat LMC theoryshould applyto eimeriorin intestinal parasites. Aspredicted, datafrom 13eimeriorin species showeda female- biasedsex ratio, with the sexratios suggesting high levels of sel¢ng (0.8^1 .0).Importantly,ourestimate of the sel¢ng rate inone of these species, Toxoplasma gondii, isinagreement with previous genetic analyses. In contrast, wepredict that LMC theorywill not apply to the groupsin which syzygy occurs (adeleorins, gregarinesand piroplasms) .Syzygyoccurs whena singlemale gametocyte and a singlefemale gameto - cyte pairtogether physically or in close proximity ,just priorto fertilization. As predicted, datafrom four adeleorinspecies showedsex ratios not signi¢ cantly di¡ erent from0.5. Keywords: gametocytes; Plasmodium;sel¢ng ;syzygy; Toxoplasma; virulence complete outcrossing( s 0)to 0 forcomplete sel¢ng 1.INTRODUCTION ˆ (s 1),the latter interpreted asmeaning that afemale ˆ Aspects ofparasite population structure, such assel¢ ng shouldproduce the minimum number ofsons required to rate andthe number ofgenotypes infecting each host, fertilize allof her daughters.Thisis oneof the most quanti- haveconsequences for the evolutionof drug resistance tativelyveri¢ ed aspects ofevolutionary biology (Charnov (Mackinnon& Hastings 1998),parasitevirulence (Herre 1982;Godfray 1 994;Herre et al. 2000).Severalrecent 1993;F rank1 996),disease diagnosis(Tibayrenc et al. studies haveapplied LM Ctheorysuccessfully tomalaria 1990;Hastings &Wedgwood-Oppenheim1 997),andthe andother closelyrelated blood parasites (Read et al. 1992, developmentand assessment ofvaccines and curative 1995;Pickering et al.2000).However,the evidencelinking drugs(Dye 1992;Gupta et al.1997).Despite considerable the sel¢ng rate andsex ratio is notperfect (Schall1 989; recent attention,the populationstructure ofparasitic Paperna& Landau1 991;Shutler et al. 1995)and so it isstill protozoaspecies, andin particular estimates ofsel¢ ng notclear how widely sex-ratio theory can be used toesti- rates, haveremained highly controversial (Tibayrenc mate populationstructure inparasites. 1995).Thiscontroversy has arisen in part because much Inthis paper,wegeneralize the applicationof sex alloca- previousevidence has come fromindirect genetic tiontheory across parasiticprotozoa in the phylumApicom- measures such aslinkage disequilibrium, which are open plexa.This cosmopolitan phylum consists entirelyof tomultiple explanations(Paul & Day1 998).However, parasites,and includes a number ofspecies ofmedicaland direct geneticmeasures areextremely laboriousand veterinaryimportance such asmalariaparasites ( Plasmodium expensiveto obtain (Paul et al. 1995),andso there is a spp.),piroplasms( Babesia spp.cause babesiosis in humans needfor more accessible indirect methods. andred waterfever in cattle, and Theileria spp.cause East Sexallocation theory o¡ ers atoolfor inferring sel¢ ng Coastfever in cattle) ,adeleorins( Hepatozoon spp.cause an rates innatural populations of parasites (Read et al. 1992). oftenfatal hepatozoonosis in dogs) and coccidia (various If matingtakes place between the o¡spring of one or a species of Cryptosporidium , Eimeria, Isospora, Neospora, fewmothers (asubdivided population) ,then afemale- Sarcocystis andToxoplasma arepathogenic to immunocompro- biasedsex ratio (where sexratio is de¢ned as the propor- mised humansor are the causativeagents of veterinary tionof males) is favouredby a process termed localmate coccidiosis).Our speci¢c aims areto: (i) maketheoretical competition(LM C;Hamilton1 967).Thisfemale bias predictionsfor when sel¢ ng should (and should not) lead to arises becauseit reduces competitionamong brothers for biasedsex ratios in apicomplexan species; (ii) test these mates, andbecause it increases the number ofmates for theoreticalpredictions; and (iii) use the sex-ratiodata to eachof the mother’s sons (Taylor1 981).Theoptimal sex estimate sel¢ng levels in apicomplexan species. ratio (r*)canbe shown to depend upon the sel¢ng rate (s;de¢ned as the proportionof a mother’s daughtersthat 2.BACKGROUND BIOLOGY arefertilized byher sons) bythe equation r* (17s)/2 ˆ (Hamilton1 967).Theoptimal sex ratio favoured by Thephylum Apicomplexa, class Sporozoasida,can be naturalselection shouldthus declinefrom 0.5for dividedinto ¢ vetaxonomic groups following R oberts & Janovy( 1996).Thegregarines (subclass Gregarinasina) *Author forcorrespondence ([email protected]) . aregenerally one-host parasites ofinvertebrates. The Proc. R.Soc.Lond. B (2000) 267, 257^263 257 © 2000The RoyalSociety Received 14September 1999 Accepted 4November1 999 258S. A.West andothers Sexratios of protozoan parasites adeleorins(subclass Coccidiasina,suborder Adeleorina) Theproduction of gametocytesand the process offerti- areone-host parasites ofinvertebrates orvertebrates, or lizationoccur by di¡ erent means ina varietyof host two-hostparasites that alternatelyinfect haematopha- tissues dependingon which of the ¢vemajor groups of gous(blood-feeding) invertebrates andthe bloodof Apicomplexaa particularspecies belongsto. F orthe vertebrates. Allspecies ofpiroplasms (subclass Piroplas- purposes ofthis paper,there is animportant distinction masina)are two -host parasites infectingticks and betweenthe groupsin which syzygy occurs (gregarines, vertebrates. Haemospororins(subclass Coccidiasina,sub- adeleorinsand piroplasms) and those inwhichit doesnot orderHaemospororina) ,oftenknown as the malaria (haemospororinsand eimeriorins) .Syzygyis de¢ned as parasites, aretwo-host Apicomplexa that parasitize the process wherebya singlemale gametocyte and a blood-feedingdipteran £ ies andthe bloodof various singlefemale gametocyte pair together physically or in tetrapodvertebrates. Finally,the eimeriorins (subclass close proximity,either inhost cells orinthe lumenof host Coccidiasina,suborder Eimeriorina) ,frequentlycalled organs,just priorto gametogenesis (Barta 1 999).The the coccidia(although this term is oftenused toinclude crucialconsequence of syzygy is that gametes from a the adeleorins),area diverse groupthat includesone- singlemale gametocyte are only able to fertilize the host species ofinvertebrates, two-host species ofinverte- gametefrom a singlefemale gametocyte. The excess of brates, one-hostspecies ofvertebrates andtwo -host malegametes die.In contrast, inspecies wheresyzygy species ofvertebrates. doesnot occur, sexual development involves gametes Apicomplexanlife histories involvethe alternationof pairing.In this case, di¡erent gametes arisingfrom a sexualand asexual reproduction, and the features rele- singlemale gametocyte are able to fertilize gametes vantto understanding their sexallocation can be arisingfrom a number offemalegametocytes. summarized asfollows(Roberts &Janovy1996) .Haploid infectivestages calledsporozoites infect host tissues to 3.SEX ALLOCATION IN THE APICOMPLEXA: formfeeding stages calledtrophozoites. These stages THEORETICAL PREDICTIONS undergoa periodof asexual proliferation and become multicelled stages calledmeronts (orschizonts) .These (a) Species withoutsyzygy rupture toproduce merozoites, some orall of whichtrans- Sex-ratiomodels havebeen developed previously for forminto sexual stages, whichare termed gametocytesfor malariaand related haemospororin parasites where the haemospororinsand eimeriorins, andgamonts for the fertilizationoccurs inthe bloodmeal of the invertebrate gregarines,adeleorins and piroplasms. F orthe purposes host (Read et al. 1992,1 995;Dye &Godfray1993; ofconsistency among groups of Apicomplexa and also Pickering et al. 2000).Inthese species, gametes competing withprevious malaria parasite sex-ratio papers, we refer formatings will generally be those foundin a singleblood togamonts as gametocytes. In the gregarinesand piro- meal,and so mating will occur between the di¡erent para- plasms, gametocytesare thought to be isogamous, and so site genotypes(clones) that arein asinglehost (andprodu- wecannot present sexallocation data. However ,inmost cinggametocytes) rather thanthose foundin many hosts. species ofthe other three groups,the gametocytesare Thisleads to the potentialfor LMC andsel¢ ng ifthere are sexuallydimorphic. lownumbers ofparasitegenotypes infecting each host. Inthese three groups(adeleorins, eimeriorins and Wesuggestthat the naturalhistory of eimeriorin haemospororins),`male’microgametocytes rupture to species wherefertilization occurs inthe intestines ofthe release anumber ofmale gametes, while`female’ macro- host shouldalso lead to LMC andappreciable levels of gametocytesgive rise toa singlefemale gamete. W ewill sel¢ng. As with the species wherefertilization occurs in refer tomicro- ormacrogametocytes and micro -or the blood,this shouldoccur when low numbers
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