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Sex Differences in Parasitic Infections Among Arthropod Hosts: Is There a Male Bias? Author(S): Letitia A

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Sex Differences in Parasitic Infections Among Arthropod Hosts: Is There a Male Bias? Author(S): Letitia A Nordic Society Oikos Sex Differences in Parasitic Infections among Arthropod Hosts: Is There a Male Bias? Author(s): Letitia A. D. Sheridan, Robert Poulin, Darren F. Ward and Marlene Zuk Reviewed work(s): Source: Oikos, Vol. 88, No. 2 (Feb., 2000), pp. 327-334 Published by: Wiley-Blackwell on behalf of Nordic Society Oikos Stable URL: http://www.jstor.org/stable/3547028 . Accessed: 21/08/2012 12:51 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp . JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. Wiley-Blackwell and Nordic Society Oikos are collaborating with JSTOR to digitize, preserve and extend access to Oikos. http://www.jstor.org OIKOS 88: 327-334.Copenhagen 2000 Sex differencesin parasiticinfections among arthropod hosts: is therea male bias? Letitia A. D. Sheridan,Robert Poulin, Darren F. Ward and MarleneZuk Sheridan,L. A. D., Poulin, R., Ward, D. F. and Zuk, M. 2000. Sex differencesin parasitic infectionsamong arthropod hosts: is there a male bias? - Oikos 88: 327-334. A highersusceptibility to diseases or parasites in males than femalesmay be an ultimateconsequence of the differentreproductive strategies favored by selectionin the two sexes. At the proximatelevel, the immunosuppressanteffects of testosterone in vertebratesprovide a mechanismthat can cause male biases in parasiteinfections. Invertebrates,however, lack testosteroneand other steroidhormones. We used a meta-analysisof published results to investigatewhether sex biases in parasite infectionswere generally observed among arthropodhosts despite the absence of the immune-endocrinecoupling provided by testosterone.Overall, male and female arthropodsdid not differin prevalenceor intensityof parasite infections.This is based on an analysisof sex differencescorrected for sample size and, whenpossible, variabilityin the originaldata. Sex biases in parasiteinfection were not more likely to be observedin certainhost or parasite taxa, and were not more pronouncedin experimentalstudies than in surveysof naturallyinfected hosts. Our resultssuggest that because of the absence of endocrine-immuneinteractions in arthropods,males are not generallymore prone to parasiteinfections than femalesdespite the greater intensityof sexual selectionacting on males. L. A. D. Sheridanand R. Poulin (correspondence),Dept of Zoology, Univ.of Otago, P.O. Box 56, Dunedin,New Zealand (robert.poulin(stonebow.otago.ac.nz).- D. F. Ward,School of Zoology,La Trobe Univ.,Bundoora, Victoria 3083, Australia.- M. Zuk, Dept of Biology,Univ. of California,Riverside, CA 92521, USA. Ultimately,most if not all differencesbetween the sexes literaturesurveys have found small but consistent male are theproduct of sexualselection (Clutton-Brock and biasesin infectionsby helminthand arthropodpara- Parker1992, Owens and Thompson1994). In most sitesin birdsand mammals(Poulin 1996a, Schalk and species,males invest in costlysecondary sexual features Forbes 1997). The proximatemechanism most often or courtshipdisplays to attractfemales, while at the associatedwith male-biased parasitic infection is the same timecompeting intensely with other males for immunesuppression associated with androgens, pri- access to females.This resultsin greaterinter- and marilytestosterone, the hormonesnecessary for the intrasexualselection pressures on malesthan females, developmentof malesexual traits and behavior(Gross- withthe life of a malebeing more socially and energet- man 1985,Alexander and Stimson1988, Schuurs and icallystressful than that of a female.One consequence Verheul1990, Zuk 1990, 1996, Folstad and Karter of thismight be thehigher mortality incurred by males 1992). In contrast,female oestrogens may actually in manytaxa (e.g. Promislow1992, Promislow et al. boosthumoral immunity (Grossman 1985). These hor- 1992). mone-mediateddifferences between the sexes can pro- Anotherconsequence might be the higherparasite duce males that are relativelymore susceptibleto infectionlevels commonly observed in the males of parasiteinfections than females. In nature,sexual dif- many vertebratespecies relative to females.Recent ferencesin susceptibilityto parasites may be maskedto Accepted 19 May 1999 CopyrightC) OIKOS 2000 ISSN 0030-1299 Printedin Ireland - all rightsreserved OIKOS 88:2 (2000) 327 somedegree by differencesin exposureresulting from collectionand our own data sets. Most of the data sex-specificbehaviors (e.g. see McCurdyet al. 1998). (88% of themale-female comparisons used) came from Thusthe proximate effect of sex hormones on suscepti- studiesthat did not focuson sex biasesin parasitism bilityto parasitesis moreeasily detectable in experi- butreported these data nonethelessfor descriptive pur- mentalstudies, where exposure is controlled,than poses.It is thereforeunlikely that our data setsuffered amongnaturally infected males and females(see Schalk froma problemof under-representationof non-signifi- and Forbes1997). cantdifferences. The bulkof theresearch carried out thusfar on sex Two measuresof parasitismwere consideredand biasesin parasitismhas beenperformed on vertebrates,recorded separately for each sex: prevalence (percentage and almostnothing is knownof thegeneral patterns of hoststhat are infected)and intensity(mean number and processesin invertebrates(Zuk and McKean1996). ofparasites per infected hosts). To be included,a study On the one hand, the operationof sexual selection had to reportprevalence and/or intensity of infection shouldbe the same in invertebratesas in vertebratesby a parasitespecies and samplesizes for both sexes of (Clutton-Brockand Parker1992), ultimately producing a hostspecies. If available,we also recordedthe stan- differentreproductive strategies in malesand females darddeviation in intensityfor both males and females. and causingsex biasesin parasiteinfections. On the Finally,we only kept studiesin whichthe typeof otherhand, the proximatemechanism operating in infection(experimental or natural)was clearlystated. vertebrates,i.e. theimmunosuppressive effects of testos- Some studiesprovided more than one comparisonto terone,is absentin invertebrates.The relationshipbe- the data set. A totalof 33 studiescontributed to the tweensex and parasiteinfections may therefore be less data set(see Appendix1). likelyto developin invertebrates(Zuk and McKean 1996).However, other mechanisms could produce sex biasesin parasiteinfections among invertebrates. For instance,males may have less energyto investin im- Statisticalanalysis muneresponses than females because males engage in We treatedeach host-parasitespecies combination as intrasexualcompetition and courtshipof females.It an independentobservation. While phylogenetic effects wouldbe importantto quantifythe general pattern of mayinfluence sex biases in infection(Harvey and Pagel sex biasesin parasitismamong invertebrate species to 1991),it is difficultto controlsimultaneously for both determinewhether the expected ultimate effects of sex- thehost and parasite phylogenies. Previous meta-analy- ual selectionon parasiteinfections also occurin taxa ses of sex biasesin parasiteinfections have similarly thatlack testosterone and othersteroid hormones (Zuk treatedeach host-parasitecombination as statistically and McKean 1996). independent(Poulin 1996a,Schalk and Forbes 1997, The objectiveof this studywas to investigatethe McCurdyet al. 1998). occurrenceand generaldirection of sex biasesin para- Comparisonsof prevalence and intensityof infection siteinfections among arthropod species. We performedbetween the sexes were computed for each host-parasite a meta-analysisof publisheddata on maleand female systemto producestandard measures that are indepen- infectionlevels in whichwe controlledfor sample sizes dentof samplesize (Hedgesand Olkin 1985).Differ- as well as assessingthe influenceof othervariables. encesin prevalencewere calculated as Theseother variables were host and parasitetaxonomy andwhether the hosts had beennaturally or experimen- where J 1 - [3/(4(Nf+ Nm -2) - tallyinfected by theparasites. We examinedthe effect (pf-Pm)(J), 1)] ofthese variables because sex biases in parasitism might be morelikely to developin certainhost taxa infected The differencebetween the prevalencein females,pfp by certainparasite taxa, or moreeasily detected when and thatin males,PM, is weighedby J, whichis a exposureis experimentallycontrolled. correctionfor small sample sizes, Nf and Nm.As the totalsample size increases,J approachesone so that moreweight is givento comparisonsbased on many hostindividuals (Hedges and Olkin1985). This correc- Methods tionis importantbecause estimates of prevalenceare ofteninfluenced by host samplesize (Gregoryand Data collection Blackburn1991). Using the above formula,we get We searchedthe literature for data on fungal,proto- positivecomparisons when prevalence is greaterin fe- zoan or metazoaninfections in femalesand malesfrom males,and negativecomparisons when it is greaterin thesame natural population or fromthe same experi- males.Similarly, differences in intensity were computed mentalstudy. Specifically, we searchedall issues of as Parasitologyand theJournal of Parasitologyavailable at the Universityof Otago, as well as RP's
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