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Reproductive Isolation Driven by the Combined Effects of Ecological

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Reproductive Isolation Driven by the Combined Effects of Ecological Received 28January 2003 Accepted 14 May 2003 Publishedonline 25 July 2003 Reproductive isolationdriven bythe combinedeffects of ecologicaladaptation and reinforce ment P. Nosil1* ,B.J.Crespi 1 and C.P.Sandoval 2 1Departmentof Biosciences, BehavioralEcology Research Group, 8888 University Drive,Simon FraserUniversity, Burnaby, BritishColumbia V5A 1S6, Canada 2MarineScience Institute, University ofCalifornia, Santa Barbara, CA 93206,USA Recentyears have seena resurgenceof interestin theprocess of speciationbut few studies have elucidated themechanisms either driving or constraining theevolution ofreproductive isolation. In theory, thedirect effectsof reinforcing selectionfor increasedmating discrimination whereinterbreeding produceshybrid offspring with lowfitness and the indirect effectsof adaptation todifferent environments can both promote speciation.Conversely, high levels ofhomogenizing geneflow can counteract the forces of selection. We demonstratethe opposing effectsof reinforcing selectionand gene flow in Timema cristinae walking-stick insects.The magnitude offemale mating discrimination against males from other populations is greatest whenmigration rates betweenpopulations adaptedto alternate hostplants are high enoughto allow the evolutionof reinforcement, but low enough to prevent gene flow from eroding adaptive divergencein mate choice.Moreover, reproductive isolation is strongestunder the combined effects of reinforcement andadaptation toalternate hostplants. Our findingsdemonstrate the joint effects of reinforcement, eco- logical adaptation andgene flow on progress towardsspeciation in thewild. Keywords: geneflow; hybridization; natural selection;speciation; Timema;walking-stick insects 1. INTRODUCTION distributedthroughout westernNorth America (Crespi& Sandoval 2000). Timema cristinae exhibits twogenetically Speciation via natural selectioncan occur as an indirect determinedcolour-pattern morphs (Sandoval 1993), with by-productof adaptive divergence(Mayr 1963; Jiggins et an unstripedmorph being more commonon thehost plant al. 2001) andcan also involve directselection for repro- Ceonothusspinosus anda stripedmorph being more com- ductiveisolation in geographical regions wherehybridiz- mon on Adenostomafasciculatum (Sandoval 1994 a). Pre- ation is maladaptive (i.e.reinforcement) (Dobzhansky dation on T.cristinae by birds andlizards is strong and 1951; Howard1993; Butlin 1995; Noor 1999). When eachmorph is mostcryptic onthe plant onwhich it is speciationoccurs as a by-productof adaptive divergence, more common(Sandoval 1994 a,b).Populations usingdif- ecologically divergent populations exhibit greater repro- ferenthost plants have also diverged in asuiteof other ductiveisolation than ecologically similar populations of morphological andbehavioural traits, including body size similar age (reviewedin Funk1998; Rundle et al. 2000; andshape, host preference and cryptic resting behaviour, Schluter2000; Funk et al. 2002). The key prediction of wherehost preference refers to a preferenceto rest on a thereinforcement hypothesis is that non-allopatric particular host,given thechoice (Nosil et al. 2002; Nosil & (geographically contiguousor overlapping) populations Crespi2003). will exhibit greater mating discrimination than allopatric Levelsof sexual isolation are higher betweenpairs of T. (geographically separated)populations. Previous empirical cristinae populations usingdifferent host plants ( n = 15 studiesof reinforcementhave provided evidencefor sucha pairs) than betweensimilar-aged pairs usingthe same host pattern (Noor 1995; Saetre et al. 1997; Rundle& Schluter plant (n = 13 pairs) (Nosil et al. 2002). Becauseinsect col- 1998; Higgie et al. 2000) butthere are fewdata onhow ourmorph (stripedversus unstriped) does not influence ecological adaptation andreinforcement interact during between-populationmate choice,the sexual isolation that thespeciation process (Schluter 2000). Furthermore, has evolved betweenpopulations adaptedto alternate although theoretical modelspredict that theoutcome of hostsis independentof colour pattern (although colour reinforcementreflects a balance betweenthe strength of pattern might influencewithin-population mate choice; reinforcing selectionand the ability ofhomogenizing gene Nosil et al. 2002). In this study,we expand previous work flowbetween populations tocounteract selection by consideringthe effects of reinforcing selectionand gene (Sanderson1989; Servedio& Kirkpatrick 1997; Cain et flowon between-population mating preferences. al. 1999; Servedio2000), this prediction has never,to our Timemacristinae satisfiesall ofthe preconditions for knowledge,been tested using natural populations. reinforcementto contribute to the reproductive isolation In this paper, weuse Timema walking-stick insectsto observedbetween populations. First, interbreeding and analyse thejoint roles ofecological adaptation, reinforce- geneflow between adjacent populations usingdifferent mentand gene flow in theevolution ofreproductive iso- hostplants (i.e.‘ hybridization’between the host-adapted lation. Timema are winglessphytophagous insects forms)is strongly suggestedby theobservations that indi- viduals from adjacentpopulations ondifferent hosts are well within oneper-generation dispersal distanceof each *Authorfor correspondence ([email protected]). other (Sandoval 1993, 1994 a)andthat between-morph Proc.R. Soc.Lond. B (2003) 270, 1911–1918 1911 Ó 2003 TheRoyal Society DOI10.1098/ rspb.2003.2457 1912P. Nosil andothers Natural selection andspeciation matings are commonin naturewhere populations using differenthosts are in contact(Nosil et al. 2002). More- over,geographical variation in morphology is indicative of parapatric 1 abalance betweenhost-specific selection and gene flow population A C betweenadjacent patches (Sandoval 1994 a;Nosil &Cre- C spi 2003), andthe populations are conspecific.In this allopatric study,we use mitochondrial DNA (mtDNA) sequence C variation toprovide further evidenceof interbreeding and population 2 geneflow between adjacent populations of T.cristinae . Second,the evolution ofreinforcement traditionally parapatric C A 3 requiresreduced hybrid fitness.In T.cristinae, between- population hostmigrants are more likely tobe of the locally non- C matching colourmorph than are residents(Sandoval allopatric A 1994a)andthe non-matching morph is at alarge selective population 4 disadvantage owing todifferential predation (therelative fitnessof the less-cryptic morph is 0.30; Sandoval Figure 1. Representative examplesof thefour ‘types’ of 1994a,b).Thusoffspring derivedfrom between-hostmat- between-population crosses (C, Ceonothus population; A, Adenostoma population). Eachsquare represents a ing (i.e. ‘hybridization ’)will tendto exhibit reducedfitness homogeneous patchof asingle host plant, whichmay or relative tooffspring derivedfrom within-population mat- maynot havea neighbouring population using the ing becausefemales who mate with locally less-cryptic alternative host plant (parapatric and allopatric populations, males producea higher frequencyof offspring that are the respectively). ‘Study’ populations used in mating trials are locally non-matching colourmorph or intermediate in col- represented byunfilled boxes, and blackboxes represent ourpattern (i.e.bear afaint stripe) than femalesthat mate populations thatare adjacent toastudy population but were with cryptic males (experimental geneticcrosses show that not used in mating trials. In thefigure, malesfrom allopatric Ceonothus populations are used asan illustrative example; in only 5% ofwithin-morph crossesproduce F 1 offspring of thealternate morph or intermediates,whereas 80% of themating trials malesfrom eachof the12 study between-morphcrosses produce both morphs or inter- populations were used (i.e. malesfrom allopatric and parapatric populations on eachhost). 1, femaleparapatric, mediates;Sandoval 1993). Although previous workdem- male from thesame host; 2, femaleallopatric, male from the onstratesthat femalesproducing offspring ofthe samehost; 3, femaleparapatric, male from thealternative non-matching colour-patternmorph will beat aselective host; 4, femaleallopatric, male from thealternative host. disadvantage (Sandoval 1994 a,b),thecost of producing offspring that are intermediate in colourpattern is lesswell known.In thecurrent study, we test whether selection against theintermediate colour-patternmorph also are geographically separatedfrom all other hostpatches imposesreinforcing selection,predicting that if theinter- by regions lacking suitable hosts.We define a ‘population’ mediate morph exhibits lowfitness then its frequencywill ofwalking-stick insectsas all theinsects collected within declinethrough time (i.e.between sequential time periods ahomogeneouspatch ofa single hostplant. ‘Parapatric’ andage classes;Endler 1986). Becausepopulations using insectpopulations are in contactwith apopulation of differenthosts have diverged in anumberof traits other insectsadapted to the alternate host,while ‘allopatric’ than colourpattern (Nosil et al. 2002; Nosil &Crespi populations are separatedfrom all populations adaptedto 2003), selectionagainst ‘hybrids’ may extendbeyond that thealternative hostby distancesof more than 50 timesthe basedupon colour pattern alone. 12 mper-generation gene-flowdistance (Sandoval 1993). Finally, wenote that recenttheoretical workindicates Reinforcementwould be supported by higher between- that directselection against hybrid mating canpromote population copulation frequenciesin mating trials involv-
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