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Costly Traumatic Insemination and a Female Counter-Adaptation in Bed

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Costly Traumatic Insemination and a Female Counter-Adaptation in Bed Received 18April 2003 Accepted 8 July 2003 Publishedonline 10September 2003 Costlytraumatic inseminatio nanda female counter-adaptationin bed bugs Edward H.Morrow * and Go¨ranArnqvist UppsalaUniversity, EvolutionaryBiology Centre, Department of Animal Ecology, Norbyva ¨gen18D, SE-752 36 Uppsala, Sweden Male bedbugs pierce femalesthrough thebody wall andinseminate directly into thebody cavity. It has previously beenshown that suchtraumatic insemination carries costsfor females,and sexual conflict regarding themode of insemination shouldthus propel male–female coevolution.Since males accumulate sexually antagonistic adaptations,females should evolve counter-adaptationsthat efficiently abate thecosts tofemales of sexual interactions.Yet, unambiguous experimental evidencefor female counter-adaptations is lacking. In bedbugs, the spermalege (a highly modifiedregion ofthe abdomen where the male usually piercesthe female) may representa female counter-adaptation.We assess the female costsof traumatic insemination by varying therate ofinsemination onthe one hand, and the rate andmode of piercing trauma tofemales on the other. Our resultsshow that female mating costsare notextreme— elevated mating rate shortenedfemale lifespan buthad nosignificant effecton lifetime egg production.More importantly, additional abdominal piercing in thespermalege had noeffect on females whereas even a very lowrate ofsuch piercing outsidethe spermalege reducedfemale lifetime egg productionby 50%. Thus,females are well counter-adaptedto theintrusive modeof insemination exhibited bymale bedbugs andthe costs of elevated mating are comparable with thosein other insects,as predicted by theory. We thereforedemonstrate that thespermalege efficiently reducesthe direct costs of piercing trauma tofemales, andhence provide experimental evidencefor afemale counter-adaptationto a sexually antagonistic male trait. Keywords: sexual selection;multiple mating; Cimex lectularius ;costsof mating; sperm competition; coevolutionary arms race 1. INTRODUCTION thuseffectively hiding thecosts and conflict from the observer (Chapman &Partridge 1996). Thus,counter to Differencesin theevolutionary interestsof the sexes are naive expectations,we do not expect sexual interactions rife in sexually reproducing organisms (Parker 1979; tobecome more costlyas antagonistic adaptations become Chapman &Partridge 1996; Rice1996, 2000). Suchsex- more escalatedin agiven sex,because matching counter- ual conflictis predictedto lead tocoevolutionary ‘arms adaptations will occurin theother sex(Arnqvist &Rowe races’between the sexes (Parker 1979; Rice& Holland 2002a).Nevertheless,convincing empirical (Rice1996) 1997). Sucharms racesproceed over evolutionary time andcomparative (Arnqvist &Rowe2002 a)evidencenow whereadaptations in onesex select for counter- existsto demonstrate that sucharms racesdo occur. adaptations in theother sex,where the latter are aimed at Male bedbugs (Heteroptera; Cimicidae) donot copu- ameliorating thecosts imposed by theformer. Thus,as late via thegenital opening ofthe female. Instead they Dawkins& Krebs(1979, p.57) phrasedit, ‘asswords get pierce thefemale abdominal wall with their sharp intro- sharper, soshields get thicker, soswordsget sharper still’. mittent organ (paramere) andinject sperm andaccessory Sexually antagonistic coevolutionplays asignificant role gland fluidsdirectly into theblood, leaving visible melan- in theevolution ofsexual dimorphism in general (Rice izedscars (Carayon 1966). This unusualmode of copu- 1984), aswell asin theevolution of reproductive mor- lation, termedtraumatic extragenital insemination,occurs phology (Arnqvist &Rowe2002 b),physiology (e.g.semi- in only asmall numberof taxa butit is foundin all mem- nal fluid proteins;Rice 1996) andbehaviour (e.g. bersof the bed bug family (Usinger1966). In many bed courtship;Arnqvist &Rowe2002 a).It has also been bugs,the area at which themale piercesthe integument implicated asan important engineof speciation (Parker & ofthefemale showsseveral unilateral modifications called Partridge 1998; Rice1998; Arnqvist et al. 2000; thespermalege. For example, in thehuman bedbug Gavrilets 2000). Cimex lectularius aspecialized notchand a cuticular thick- Despitethe fact that sexually antagonistic coevolution ening ofthe right sideof the fifth sternite(the generatesadaptations, in both sexes,which are costlyfor ectospermalege) lies directly over adistinctpocket filled theother sex,the process is notoriously difficult todetect with haemocytoid cellson the inner surface of theabdomi- empirically. This is becausewe expect adaptation in one nal wall (themesospermalege) (Carayon 1966). sexto be balanced by counter-adaptationin theother, Mating at very high rates is costlyto female insectsin general (seeArnqvist &Nilsson2000 for areview) and bedbugs are noexception (Stutt & Siva-Jothy 2001). *Authorand address for correspondence: Department of Ecology, Evolution& Marine Biology,University of California SantaBarbara, CA Despitethe apparently damaging natureof traumatic 93106,USA ([email protected]). insemination,we do not expect male– female interactions Proc.R. Soc.Lond. B (2003) 270, 2377–2381 2377 Ó 2003 TheRoyal Society DOI10.1098/ rspb.2003.2514 2378E. H.Morrowand G. Arnqvist Costsof traumatic insemination in bedbugs to carry extreme costsfor tworeasons. First, (b) Experimental treatments becauseof continual sexually antagonistic coevolution, Weindependentlyvaried the followingfactors: (i)the rate of femalesshould be well counter-adaptedto copewith any insemination;(ii) the rate of piercingtrauma; (iii)the siteof damaging effectsof mating. The spermalege is an obvious piercingtrauma; and (iv)the probability of infectionduring candidatefor sucha female counter-adaptation.The evol- piercingtrauma. The first variablewas based upon mating utionof the spermalege within theCimicidae wasfirst regime,using two treatments. Femaleswere either housed with consideredby Carayon (1966) whoexplicitly suggested four virginmales (high mating rate)or were housed with four that thespermalege evolved toreduce direct costs to virginmales, three of which had had theirparamere glued into femalesassociated with thetrauma ofinsemination (see the parameregroove (lowmating rate),using asmallamount of also Stutt& Siva-Jothy 2001). Suchcosts may include:(i) quick-dryingglue (Super Attak, Loctite).This gluingtreatment repair ofthewounded cuticle; (ii) leakage ofhaemolymph; had no observable effecton malebehaviour. The lattertreat- (iii) increasedrisk ofinfection through thepuncture mentcontrols for any confoundingeffects of exposure to males wound;and (iv) immune defenceagainst sperm oraccess- ormaleharassment, thus isolatingthe effectof copulation,since ory gland fluidsthat are introduceddirectly into theblood threeout of the four maleswere unable actually to copulate. ofthe female. The protectionafforded by thespermalege Any malesthat diedduring the periodof the experimentwere tothe female during andafter copulation may operate in replacedwith amaleof the sametype (gluedor normal). Each anumberof ways:(i) by localizing damage toone area on replicateof four malesand asinglefemale was housed inawell theabdomen; (ii) by restricting thediffusion of theejacu- (volumeof 6ml)of amodifiedcell-culture plate fittedwith a late insidethe female; (iii) by reducingleakage ofblood gauze panelin the lid.A smallslip of filterpaper was provided through thewound site; and (iv) by restricting entry of as an ovipositionsubstrate. Femaleswere included in the experi- pathogensinto thebloodstream. It shouldbe noted, how- mentuntil their death. ever,that thedegree of elaboration ofthe spermalege var- Inaddition to the trauma experiencedduring mating, all iestremendously across different heteropterans exhibiting femaleswere subjected to additionalexperimentally imposed traumatic insemination (Carayon 1966). abdominalpiercing trauma. Femaleswere either: (i) simply Second,all elsebeing equal,males will sufferfrom handledfor the sameamount of timethat the treatments below harming their mates(Parker 1979). There shouldthere- took to complete( ca.1min);(ii) pierced through the ectosperm- forebe selection in both sexesto reduce the direct costs alegewith asterilizedpin (rinsed briefly in 98% ethanol and oftraumatic insemination tofemales, favouring males that allowedto dry priorto piercing);(iii) pierced through the ectos- inseminatefemales in alesscostly manner andleaving permalegewith anon-sterilizedpin that, priorto piercing,had only thosecosts that are more or less ‘unavoidable ’ to per- beenwiped over the surfaceof acontaminatedfilter paper taken sistover evolutionary time (seeHosken et al. 2003; Mor- froma jar containinga bedbug colony;(iv) pierced outside of row et al. 2003). For thesereasons, the costs of mating in the spermalegewith asterilizedpin, through the integument bedbugs should not be extraordinary. betweenthe fifth and sixth segments of the ventralsurface of The purposeof this reportedwork is twofold.By inde- the abdomenon the leftside of theirbody. This positionmirrors pendentlyvarying therate ofinsemination andthe type of exactly the positionof the ectospermalegeon the ventralsurface puncturetrauma in abedbug species,we first quantify ofthe right sideof the femaleabdomen. These treatments were female mating costsand second we dissectthe proximate carriedout oncea week,and allowedus to evaluatestatistically causesof such costs. We predict that thecosts of mating the effectson femalesof rate of piercingtrauma, siteof piercing shouldnot be dramatic.
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