- Email: [email protected]
Adaptive genetic structure in phytophagous insect populations
REVIEWS
Adaptivegenetic structurein phytophagous insect populations Susan Mopper and ovipositional preferences restrict gene flow and facilitate rapid local evolution through a combination of genetic drift and natural selection. Perhaps the most compelling evidence for sympatric race formation is from the economically important apple maggot fly (Rhagoletis pomone/la)llJ*-20. There are two sympatric races in the population, one that feeds on hawthorn (Crataegus spp.), the native North American host, and one that specializes on the introduced, domesticated European apple (Malus pumila). In a series of mark-andrecapture experiments, adult flies displayed strong fidelity to the plant species of natal origin. Such host fidelity encourages further evoluSusan Mopper is at the Dept of Biology, tion of plant-related adaptations University of Southwestern Louisiana, that may eventually lead to reproLafayette, LA 70504-2451, USA ductive isolation between the races. ([email protected]). In this system, both host preference and timing of adult eclosion are pre-mating barriers to gene thus are adaptive in flow. Allozyme analysisigJ1 confirms the existence of two sympatric, yet genetically divergent fly races, although gene exchange between them is approximately 6% per generation per year (Ref. 18). In the absence of strong counterbalancAdaptive evolution within and among populations The role of the host plant ing selection, gene flow of this magnitude could rapidly homogenize the population and eliminate genetic structure. The evolution of genetically distinct races within single There are at least three adaptive advantages associated populations appears widespread among polyphagous insects feeding on multiple host plantsiz. The unique selection with the new apple host: (1) apples provide greater strucpressures associated with each plant species leads to reprotural protection from parasitism by hymenopteran wasps; ductive isolation and eventually sympatric race formation in (2) interspecific competition with other larval insects is less the insect population, despite the overlapping distributions frequent; and (3) earlier apple flowering phenology provides a temporal window of escape from parasitismzo. Although of host-plant species. Though much of our current knowledge is based on economically important pests such as the fall larval feeding performance is greater on the ancestral hawarmyworm (Spodopfera t?ugiperda)l3, the pea aphid (Acyrthothorne than the introduced apple in both fly races, it is siphon pisum)l4, the apple maggot fly (Rhagoletis pomonella)ll counterbalanced by the enemy-free space provided by apple hosts. The trade-off between larval performance and paraand the eastern tent caterpillar (Malacosoma americanum)l5, the following studies indicate that natural insect populations sitism maintains a stable polymorphism in the Rhagoletis population. also display fine-scale evolutionary divergence in association with host plants. The role of behavior The rapid diversification of endemic soapberry bug (Jadera haematofoma) populations occurred in response to The widely distributed eastern tent caterpillar (Ma/aplants recently introduced to North Americalc. In less than cosoma americanurn) exemplifies how behavior can hom50 years, adaptive evolution in beak length paralleled variogenize genetic variation at both micro and macro spatial ation in fruit size of three new host-plant species. In another scaleW2. Malacosoma americanum displays strong fidelity North American native, Euphydryas editha, a checkerspot to the patchily distributed black cherry (Prunus serotina) butterfly, human disturbance has endangered natural popuin a broad range of heterogeneous environments, yet there lations of Colfinsia paruiflora, the primary hostir. Since 1983, is little evidence of genetic divergence among widespread some butterflies have included a new host in their diet, the populations of this caterpillar. In a series of studieW* spanintroduced European weed, Plantago lanceolata. In the past ning from local demes to populations, there was a striking decade, the proportion of butterflies that actively prefer the lack of genetic structure that may be owing to the unique introduced host plant has risen sharply. It is likely that the social biology of the moth. Through group shelter construction and thermoregulation, M americanum larvae create checkerspot’s sedentary dispersal behavior, diet selection opulation genetic structure is determined by genetic isolation, which is governed by the forces of genetic drift, natural selection and gene flow’. Gene flow acts to homogenize the genetic diversity that natural selection and drift promote. In natural insect populations, isolating factors such as dispersal ability, population age, habitat patchiness and host-plant longevity can counteract the effects of gene flow and produce genetic structure at fine spatial scales2. Demes are distinct yet contiguous groups of interbreeding organisms that form as a result of genetic isolation despite proximity to organisms of the same species3!4. Intrapopulation deme formation is well-documented in such diverse insect taxa as Coleoptera5J, Homopterar78,Thysanopterag, Lepidopteraio and DipteralI. This paper will focus primarily on demes that evolve sympatrically in response to natural selection, and nature.
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Genetic variation in insect populations is frequently structured into discrete groups, or demes, that form in response to stochastic forces or natural selection. Because host-plant populations are often highly heterogeneous, phytophagous insects may form demes that are adapted to the unique traits of individual plants. Recent field experiments indicate that selection pressures imposed by host-plants can promote rapid adaptive evolution in natural insect populations at very fine spatial scales. Adaptive deme formation may be more common among endophagous insects, which feed and reside within plant tissue, than for externally feeding insects, because internal feeders experience stronger plant-mediated selection pressures.
0 1996, Elsevier Science Ltd
PII: SO169-5347(96)1003&7
23 5
REVIEWS scale demic structure in the insect population. The first experimental Host plant Mobility Deme formation Insect test of the hypothesis was conducted by Edmunds and Yes ponderosa pine sessile Black pineleaf scale Alstad25 in a natural popu(Pinus ponderosa) (Nuculaspis ca/ifornica)25 lation of black pineleaf scale II I, “37 No sugar pine (Nuculaspis califomica) inhabit(Pinus lambertiana) ing ponderosa pine (Pinus n ponderosa). To test the deme Yes beech Beech scale formation hypothesis, the (Fagus sy/watica) (Cfyptocc~ccus fagisuga) 36 investigators transferred in81 seaside daisy Yes Thrips sects among natal and novel (Erigeron glaucus) (Apterothrips secticornis)g plants, then evaluated insect 1. performance. Higher scale mulberry Yes Armored scale (Morus alba) survival on natal plants com(Pseudaulacaspis pentagona) pared with novel plants indiI, No pinyon pine Needle scale cated the presence of locally (Pinus edulis) (Matsucoccus acalyptus) 33 adapted demes at the spatial II II II ” “34 scale of individual trees. No Allozyme markers later conYes Leafminer sand-live oak dispersive firmed tree-level genetic struc(Quercus geminata) (Stilbosis quadricustatella) 10 ture of N. califomica, in adI, dition to genetic structure sea oxeye daisy Yes Gall midge (Borrichia frutescens) (Asphondilia borriChia)38 among insects occupying different branches of the same I, mountain birch No Geometrid moth trees. (Betula pubescens) (Epirrita autumnata)aQ Adaptive deme formation remains a controversial theory because of flaws in the origand the division between the studies testing environments that mitigate the extensive latitudinal and alti- inal study25,33,34 tudinal gradients encountered throughout their range. Cen- the hypothesis (Table 1). Six of the ten field tests of the hypothesis support the theory (Table 1). An experiment etic variation at 11 polymorphic loci support the assumption that behavioral and social buffering of the environment prewith thrips insects is a convincing exampleg. Thrips (Apterothrips secticomis) displayed higher growth rates when vents genetic isolation in this gregarious insect23. Dispersal transferred to cuttings collected from their natal plant, the and feeding behavior in the lycaenid butterfly, Euphifotes seaside daisy (Erigeron glaucus), than when transferred to enoptes, also affects population genetic structure24. Flight cuttings from novel conspecific hosts. The potentially conmobility prevents genetic isolation and differentiation by promoting gene flow in a stepwise fashion across a wide el- founding effects of environmental variation and maternal influence were eliminated from the experiment by rearing all evational gradient. thrips on novel host plants for several generations. The thrips study demonstrates fine-scale adaptive difAdaptive deme formation ferentiation of a native insect to individual plants in a popuUnlike sympatric race formation in which genetic struclation. However, other experiments failed to detect a similar ture is associated with multiple hosts, demes form within phenomenon despite the relative immobility of the inmonophagous insect populations that specialize on a single sect&34. In general, field experiments combined with alloplant species. Differentiation across narrow spatial boundzyme data indicate that local genetic structure may be a aries can be particularly apparent for insects that feed and widespread evolutionary phenomenon in specialist insect reside on long-lived host plantG5. population&Q but the forces underlying this structure, be Many phytophagous insect species produce hundreds of generations on an individual plant. Plant genotype, en- they selective or stochastic, remain unresolved. vironmental conditions and interactions between them creGene flow and adaptive deme formation ate strong selection pressures that impact insect survival, An important requirement for adaptive deme formation fecundity and population growth rates26. This is apparent is genetic isolation among insects despite their proximity. when phenotypic variation in plant traits such as nutritional Hence most experiments testing the hypothesis have emquality and/or chemical defense leads to differential herployed relatively non-dispersive organisms such as scale bivory, a conspicuous feature in many natural plant popuinsects, and these studies are about evenly divided in suplations including Rhus27, Salix28, Populus29 and Quercus30. porWJ5J6 and rejection33J4J7 of the hypothesis (Table 1). Variation among trees in quality, natural enemy distribution, Even minimal gene exchange can prevent the evolution of and herbivore social interactions probably produced treelevel genetic structure in willow leaf beetle populationGJ2. locally adapted demes. Hanks and Denno detected local adap tation in the highly sessile armored scale only when the host Extreme differential herbivory inspired the adaptive mulberry trees were isolated by more than 300 m (Ref. 35). deme formation hypothesis25, which predicts that insects However, gene flow per se is a poor predictor of deme forquickly adapt to the phenotypic traits of individual host mation. Three studies examined deme formation in dispersive plants. The theory predicts that as insects repeatedly coloninsect&BJg, and two reported adaptive genetic variation at ize the natal host, they become more successful at exploiting the spatial scale of individual host plantslOJ8.In the disperit and less successful at exploiting novel conspecific plants. After several generations, natural selection produces fine- siveSti/bosis quadricustatella leafminer population, adaptive Table 1. Experimental tests of the adaptive deme formation hypothesis
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REVIEWS variation occurred on experimental trees growing from lo-150m apartlo. A recent field experiment suggests that adult .S.quadricustutefIa females selectively oviposit on particular Quercus geminata trees, which may contribute to reproductive isolation in this dispersive insectso. Direct estimates of gene flow (reviewed by Peterson and Denno2) further illustrate that dispersal abilities alone do not determine the magnitude of isolation among individuals in a population. lntrapopulation genetic isolation and structure, despite high potential gene flow may necessitate correlations between genes promoting physiological adaptations and genes promoting reproductive isolation, via mechanisms such as pleiotropy or linkage 1,40.Estimates of gene flow, in conjunction with the deme formation experiments, indicate that strong selection pressures can and do counteract the effects of gene exchange, even across very narrow spatial boundaries. Agents of selection and adaptive deme formation Host plants If genetic structure appears among organisms in close proximity, what selection forces lead to it? According to the deme formation hypothesis, insects adapt to the phenotypic traits of individual trees25. A fundamental assumption of the theory is that insects inhabiting natal plants suffer less mortality from plant defense mechanisms than insects colonizing novel plants. Despite its importance to our understanding of adaptive evolution, only two studies have explicitly examined plant impacts on insect performance in the context of selection and deme formationlOJ8. Determining the cause of insect mortality can be difficult, particularly for those species that feed externally. On the other hand, endophagous insects -those that feed and reside within host-plant tissues -reveal clues about their fate. Mopper et al.10examined plant-mediated mortality among S. quadricusfate/la leafminers (Fig. 1) transferred to natal and novel sites, natal and novel host species (Q. geminatu and Q. myrtifoliu), and natal and novel Q. geminutu trees within a site. Consistent with the deme formation hypothesis, they discovered significantly reduced plant-mediated mortality in the natal treatment groups at each of the three spatial scales. Thus, although adult .S. quudricustutellu are dispersive, leafminers may adapt to individual host plants despite the potential for gene exchange among trees. Allozyme studies are currently under way to further explore genetic structure in the leafminer-oak system (K. Landau and S. Mopper, unpublished data). Stiling and Rossi also examined agents of selection in their test of the adaptive deme formation hypothesis. They presented natal and novel plants of sea oxeye daisy (Borrichiu frutescens) to ovipositing females of a gall-forming midge, Asphondyliu borrichiu and observed that gall size was significantly larger on natal plants, and adult flies preferred natal to novel plants for oviposition. Natural enemies In S. quudricustutellu leafminers, parasitism and predation can be identified by characteristic scars on the leaf. Despite reduced plant-mediated mortality on natal trees, rates of leafminer survival were similar on natal and novel treeslo. This resulted from a corresponding increase in naturalenemy mortality of leafminers inhabiting natal trees. In effect, plant- and enemy-mediated mortality were balanced such that total leafminer mortality was similar on natal and novel trees. This intriguing result suggests that natural enemies as well as their phytophagous prey may be locally adapted at TREE vol.
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the tree spatial scale. Are endophagous insects such as leafminers and gallformers more apparent to natural enemies on natal than on novel host plants? Perhaps natal inhabitants harbor superior physiological adaptations that result in more rapid growth than recent colonizers of the same plant. Faster growth may produce mines that are more conspicuous to enemies. Alternatively, natal herbivores may metabolize and excrete phytochemicals more efficiently, thereby increasing their conspicuousness to natural enemies, such as hymenopteran predators and parasitoids, which rely on chemical cues to locate prey. Implications of adaptive deme formation One discovery of the deme formation experiments and other studies of population genetic structure is that dispersal ability is a poor predictor of genetic isolation2. Highly dispersive insects can exhibit greater local adaptation than sessile insects (Table 1). These inconsistencies may be explained in part by mode of feedinglOJ8.Endophagous insects such as leafminers and gallformers are intimately associated with their host because they are confined to the same plant tissue throughout larval development. Such intimacy may magnify the selection pressures imposed by host plants and natural enemies to a degree not experienced by externallyfeeding herbivores”). Only by identifying agents of selection and mechanisms of reproductive isolation, can we understand fine-scale adaptive evolution. Long-term field experiments that identify sources of mortality are critical because insect densities, natural enemy populations, and host-plant quality can vary widely between yearsso. The field experiments should be combined with measures of gene flow and allele frequencies within and among discrete demes. Natural undisturbed insect and plant populations are often structured into discrete demes or patcheslz. Yet there has been virtually no research investigating how genetic structure in plant populations impacts genetic structure in insect populations41. Understanding the mechanisms promoting and preventing population genetic heterogeneity is important for both applied and basic science. One of the most pressing conservation issues today is the maintenance of genetic variation in rapidly shrinking natural plant and animal populations. The reduction of individual genetic variation can have devastating consequences for the entire population. The deme formation experiments described herein indicate that phytophagous insects in heterogeneous plant pop& lations are less able to exploit non-natal plants, thereby reducing the possibility of widespread contagion and insect , obtbreaksl2. Presumably, phytophagous insects can more rapidly exploit entire plant populations composed of genetically similar individuals. In a natural population of pinyon pine (Pinus e&/is), chronic insect herbivory reduced plant growth and reproduction, and was most severe for trees that were homozygous at two enzyme loci42. Without substantial genetic Fig. 1. Two active Stilbosis qua&ivariation, recombination and custatella leafminer larvae in a water oak (Quercus nigra) leaf. This photo outcrossing may not be suffigraph illustrates the intimate associcient to increase plant resistation between endophagous insects ance to adapted herbivore+u. and their plant hosts. Understanding how natural selection, gene flow and isolating I 237
REVIEWS mechanisms operate at fine-scales provides valuable insight into how evolution operates at the species level and beyond.
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Acknowledgements I thank Merrill Peterson, Peter Stiling, Sharon Strauss and two anonymous reviewers for their insightful comments on the manuscript. This research was supported by USA grants NSF BSR90-07144, EPSCoR NSF/LEQSF(19921996)-ADP-02
and LEQSF(1994-1996)-RD-A-37.
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6 Rank, N.E. (1992) A hierarchical analysis of genetic differentiation in a montane leaf beetle Chrysomefa aeneicollis (Coleoptera: Chrysomelidae), Euolution 46, 1097-l 111 7 Moran, N.A. and Whitham, T.G. (1988) Evolutionary reduction of complex life cycles: loss of host alternation in Pemphigus (Homoptera:Aphldtdae), Euotution 42, 717-728 8 Alstad, D.N. and Corbin, K.W.(1990) Scale insect allozyme differentiation within and between host trees, Euol. Ecol. 4, 43-56
9 Karban, R. (1989) Rne-scale adaptation of herbivorous thrtps to individual host plants, Nature 340, 60-61 10 Mopper, S. et al. (1995) Local adaptation and agents of mortality in a mobile insect, Euolution 49,810-815 11 Feder, J.L., Hunt, T.A. and Bush, L. (1993) The effect of climate, host plant phenology, and host fidelity on the genetics of apple and hawthorn infesting races of Rhagoietis pomonella, Entomol. Exp. Appl. 69,117-135 12 Mopper, S. and Strauss, S., eds Genetic Structure in Natural Insect Populations: Effects of Host Plants and Life History, Chapman & Hall (in press) 13 Pashley, D.P. (1988) Quantitative genetics, development, and physiological adaptation in host strains of fall armyworm, Euolution 42,93-102
14 Via, S. (1991) Specialized host plant performance of pea aphid clones is not altered by experience, Ecology 72,1420-1427 15 Costa, J.T., IIIand Ross, K.G. (1993) Seasonal decline in intracolony genetic relatedness in eastern tent caterpillars: implications for social evolution, Behau. Ecol. Sociobiol. 32,47-54 16 Carroll, S.P. and Boyd, C. (1992) Host race radiation in the soapberry bug: natural history with the history, Euolution 46, 1052-1069 17 Singer, M.C.,Thomas, C.D. and Parmesan, C. (1993) Rapid human-induced evolution of insect-host association, Nature 366, 681-683
18 Feder, J.L. et al. (1994) Host fidelity is an effective premating barrier between sympatric races of the apple maggot fly, Proc. Nat1Acad. Sci. USA91,7990-7994 19 Feder, J.L., Chilcote, CA. and Bush, G.L. (1990) Regional, local and microgeographic altele frequency variation between apple and hawthome populations of Rhagoletis pomonella in western Michigan, Evolution 44,595-608 20 Feder, J.L. (1995) The effects of parasitoids on sympatric host races of Rhagoletis pomonella (Diptera: Tephrittdae), Ecology 76, Sol-813 21 McPheron, B.A.,Courtney Smith, D. and Berlocher, S.H. (1988) Genetic differences between host races of Rhagofetis pomonella, Nature 336,64-66
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22 Costa, J.T., 111 and Ross, KG. (1994) Hierarchical genetic structure and gene flow in macrogeographic populations of the eastern tent caterpillar (Malacosoma americanurn), Euolution 48, 23 Shoemaker, D., Costa, J.T., IIIand Ross, KG. (1992) Estimates of heterozygosity In two social insects using a large number of electrophoretic markers, Heredity 69, 573-582
24 Peterson, M.A. (1995) Phenological isolation, gene flow and developmental differences among low- and high-elevation populations of Euphilotes enoptes (Lepidoptera: Lycaenidae), Evolution 49, 446-455
25 Edmunds, G.F. and Alstad, D.N. (1978) Coevolution in insect herbivores and conifers, Science 199,941-945 26 Mopper, S., Whitham, T.G. and Price, P.W. (1990) Plant phenotype and interspecific competition determine sawfly performance and density, Ecology 71,2135-2144 27 Strauss, S.Y. (1990) The role of plant genotype, environment and gender in resistance to a specialist chrysomelid herbivore, Oecologia 84, 11l-l 16 28 Boecklen, W.J., Price, P.W. and Mopper, S. (1990) Sex and drugs and herbivores: sex-biased herbivory in arroyo willow (Salk lasioiepis), Ecology 71,581-588 29 Auerbach, M. (1991) Relative impact of interactions within and between trophic levels during an insect outbreak, Ecology 72, 1599-1608 30 Mopper, S. and Simberloff, D. (1995) Differential herbivory in an oak population: the role of plant phenology and insect performance, Ecology 76,1233-1241 31 McCauley, D.E. and Eanes, W.F. (1987) Hierarchical population structure analysis of the milkweed beetle, Tetruopes tetraophthalmus (Fotster), Heredity 58,193-201 32 McCauley, D.E. et al. (1988) Spatial and temporal variation in group relatedness: Evidence from the imported willow leaf beetle, Euolution 42, 184-192 33 Unruh, T.R. and Luck, R.F. (1987) Deme formation ln scale insects: a test with the pinyon needle scale and a review of other evidence, Ecol. Entomol. 12,439-449 34 Cobb, N.S. and Whitham, T.G. (1993) Herbivore deme formation on individual trees: a test case, Oecologia 94,496-502 35 Hanks, L.M.and Denno, R.F. (1994) Local adaptation in the armored scale insect Pseudaulaspis pentugna (Homoptera: Diaspididae), Eco/ogy 75,2301-2310 36 Wainhouse, D. and Howell, R.S. (1983) intraspecific variation in beech scale populations and susceptibility of their host Fagus syluatica, Ecol. Entomol. 8,351-359 37 Rice, W.R. (1983) Sexual reproduction: an adaptation reducing parent-offspring contagion, Euolution 37, 1317-1320 38 Stiling, P.D. and Rossi, A. Deme formation in a dispersive gall-forming midge, in Genetic Structure in Natural Insect Populations: Effects of Host Plants and Life History (Mopper, S. and Strauss, S., eds), Chapman &Hall (in press) 39 Ayres, M.P., Suomela, J. and MacLean, SF., Jr (1987) Growth performance of Epirrita autumnatu mpidoptera: Geometridae) on mountain birch: trees, broods, and tree x brood interactions, Oecologia 74,450-457
40 Hanks, L.M.and Denno, R.F. (1993) The role of demic adaptation in colonization and spread of scale insect populations, in Evolution of Insect Pests. Patterns of Variation (Kim, K.C. and McPheron, B.A., eds), pp. 393-411, Wiley 41 Michalakis, Y. et al. (1993) Population structure of a herbivorous insect and its host plant on a microgeographic scale, Evolution 47, 1611-1616
42 Mopper, S. et al. (1991) Genetic differentiation and heterozygosity in pinyon pine associated with herbivory and environmental stress, Euolution 45,989-999 43 Strauss, S.Y.and Karban, R. (1994) The signtftcauce of outcrosshrg in au intimate plant-herbivore relationship. 11.Does outcrossing pose a problem for thrips adapted to the host-plant clone? Evolution 48,465-476
44 Strauss, S.Y. and Karban, R. (1994) The significance of outcrossing in an intimate plant-herbivore relationship. II. Does outcrosstng provide an escape from herbivores adapted to the parent plant? Evolution 48,454-464 TREE vol.
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Adaptivegenetic structurein phytophagous insect populations Susan Mopper and ovipositional preferences restrict gene flow and facilitate rapid local evolution through a combination of genetic drift and natural selection. Perhaps the most compelling evidence for sympatric race formation is from the economically important apple maggot fly (Rhagoletis pomone/la)llJ*-20. There are two sympatric races in the population, one that feeds on hawthorn (Crataegus spp.), the native North American host, and one that specializes on the introduced, domesticated European apple (Malus pumila). In a series of mark-andrecapture experiments, adult flies displayed strong fidelity to the plant species of natal origin. Such host fidelity encourages further evoluSusan Mopper is at the Dept of Biology, tion of plant-related adaptations University of Southwestern Louisiana, that may eventually lead to reproLafayette, LA 70504-2451, USA ductive isolation between the races. ([email protected]). In this system, both host preference and timing of adult eclosion are pre-mating barriers to gene thus are adaptive in flow. Allozyme analysisigJ1 confirms the existence of two sympatric, yet genetically divergent fly races, although gene exchange between them is approximately 6% per generation per year (Ref. 18). In the absence of strong counterbalancAdaptive evolution within and among populations The role of the host plant ing selection, gene flow of this magnitude could rapidly homogenize the population and eliminate genetic structure. The evolution of genetically distinct races within single There are at least three adaptive advantages associated populations appears widespread among polyphagous insects feeding on multiple host plantsiz. The unique selection with the new apple host: (1) apples provide greater strucpressures associated with each plant species leads to reprotural protection from parasitism by hymenopteran wasps; ductive isolation and eventually sympatric race formation in (2) interspecific competition with other larval insects is less the insect population, despite the overlapping distributions frequent; and (3) earlier apple flowering phenology provides a temporal window of escape from parasitismzo. Although of host-plant species. Though much of our current knowledge is based on economically important pests such as the fall larval feeding performance is greater on the ancestral hawarmyworm (Spodopfera t?ugiperda)l3, the pea aphid (Acyrthothorne than the introduced apple in both fly races, it is siphon pisum)l4, the apple maggot fly (Rhagoletis pomonella)ll counterbalanced by the enemy-free space provided by apple hosts. The trade-off between larval performance and paraand the eastern tent caterpillar (Malacosoma americanum)l5, the following studies indicate that natural insect populations sitism maintains a stable polymorphism in the Rhagoletis population. also display fine-scale evolutionary divergence in association with host plants. The role of behavior The rapid diversification of endemic soapberry bug (Jadera haematofoma) populations occurred in response to The widely distributed eastern tent caterpillar (Ma/aplants recently introduced to North Americalc. In less than cosoma americanurn) exemplifies how behavior can hom50 years, adaptive evolution in beak length paralleled variogenize genetic variation at both micro and macro spatial ation in fruit size of three new host-plant species. In another scaleW2. Malacosoma americanum displays strong fidelity North American native, Euphydryas editha, a checkerspot to the patchily distributed black cherry (Prunus serotina) butterfly, human disturbance has endangered natural popuin a broad range of heterogeneous environments, yet there lations of Colfinsia paruiflora, the primary hostir. Since 1983, is little evidence of genetic divergence among widespread some butterflies have included a new host in their diet, the populations of this caterpillar. In a series of studieW* spanintroduced European weed, Plantago lanceolata. In the past ning from local demes to populations, there was a striking decade, the proportion of butterflies that actively prefer the lack of genetic structure that may be owing to the unique introduced host plant has risen sharply. It is likely that the social biology of the moth. Through group shelter construction and thermoregulation, M americanum larvae create checkerspot’s sedentary dispersal behavior, diet selection opulation genetic structure is determined by genetic isolation, which is governed by the forces of genetic drift, natural selection and gene flow’. Gene flow acts to homogenize the genetic diversity that natural selection and drift promote. In natural insect populations, isolating factors such as dispersal ability, population age, habitat patchiness and host-plant longevity can counteract the effects of gene flow and produce genetic structure at fine spatial scales2. Demes are distinct yet contiguous groups of interbreeding organisms that form as a result of genetic isolation despite proximity to organisms of the same species3!4. Intrapopulation deme formation is well-documented in such diverse insect taxa as Coleoptera5J, Homopterar78,Thysanopterag, Lepidopteraio and DipteralI. This paper will focus primarily on demes that evolve sympatrically in response to natural selection, and nature.
P
TREE uol.
II,
no.
6 June
1996
Genetic variation in insect populations is frequently structured into discrete groups, or demes, that form in response to stochastic forces or natural selection. Because host-plant populations are often highly heterogeneous, phytophagous insects may form demes that are adapted to the unique traits of individual plants. Recent field experiments indicate that selection pressures imposed by host-plants can promote rapid adaptive evolution in natural insect populations at very fine spatial scales. Adaptive deme formation may be more common among endophagous insects, which feed and reside within plant tissue, than for externally feeding insects, because internal feeders experience stronger plant-mediated selection pressures.
0 1996, Elsevier Science Ltd
PII: SO169-5347(96)1003&7
23 5
REVIEWS scale demic structure in the insect population. The first experimental Host plant Mobility Deme formation Insect test of the hypothesis was conducted by Edmunds and Yes ponderosa pine sessile Black pineleaf scale Alstad25 in a natural popu(Pinus ponderosa) (Nuculaspis ca/ifornica)25 lation of black pineleaf scale II I, “37 No sugar pine (Nuculaspis califomica) inhabit(Pinus lambertiana) ing ponderosa pine (Pinus n ponderosa). To test the deme Yes beech Beech scale formation hypothesis, the (Fagus sy/watica) (Cfyptocc~ccus fagisuga) 36 investigators transferred in81 seaside daisy Yes Thrips sects among natal and novel (Erigeron glaucus) (Apterothrips secticornis)g plants, then evaluated insect 1. performance. Higher scale mulberry Yes Armored scale (Morus alba) survival on natal plants com(Pseudaulacaspis pentagona) pared with novel plants indiI, No pinyon pine Needle scale cated the presence of locally (Pinus edulis) (Matsucoccus acalyptus) 33 adapted demes at the spatial II II II ” “34 scale of individual trees. No Allozyme markers later conYes Leafminer sand-live oak dispersive firmed tree-level genetic struc(Quercus geminata) (Stilbosis quadricustatella) 10 ture of N. califomica, in adI, dition to genetic structure sea oxeye daisy Yes Gall midge (Borrichia frutescens) (Asphondilia borriChia)38 among insects occupying different branches of the same I, mountain birch No Geometrid moth trees. (Betula pubescens) (Epirrita autumnata)aQ Adaptive deme formation remains a controversial theory because of flaws in the origand the division between the studies testing environments that mitigate the extensive latitudinal and alti- inal study25,33,34 tudinal gradients encountered throughout their range. Cen- the hypothesis (Table 1). Six of the ten field tests of the hypothesis support the theory (Table 1). An experiment etic variation at 11 polymorphic loci support the assumption that behavioral and social buffering of the environment prewith thrips insects is a convincing exampleg. Thrips (Apterothrips secticomis) displayed higher growth rates when vents genetic isolation in this gregarious insect23. Dispersal transferred to cuttings collected from their natal plant, the and feeding behavior in the lycaenid butterfly, Euphifotes seaside daisy (Erigeron glaucus), than when transferred to enoptes, also affects population genetic structure24. Flight cuttings from novel conspecific hosts. The potentially conmobility prevents genetic isolation and differentiation by promoting gene flow in a stepwise fashion across a wide el- founding effects of environmental variation and maternal influence were eliminated from the experiment by rearing all evational gradient. thrips on novel host plants for several generations. The thrips study demonstrates fine-scale adaptive difAdaptive deme formation ferentiation of a native insect to individual plants in a popuUnlike sympatric race formation in which genetic struclation. However, other experiments failed to detect a similar ture is associated with multiple hosts, demes form within phenomenon despite the relative immobility of the inmonophagous insect populations that specialize on a single sect&34. In general, field experiments combined with alloplant species. Differentiation across narrow spatial boundzyme data indicate that local genetic structure may be a aries can be particularly apparent for insects that feed and widespread evolutionary phenomenon in specialist insect reside on long-lived host plantG5. population&Q but the forces underlying this structure, be Many phytophagous insect species produce hundreds of generations on an individual plant. Plant genotype, en- they selective or stochastic, remain unresolved. vironmental conditions and interactions between them creGene flow and adaptive deme formation ate strong selection pressures that impact insect survival, An important requirement for adaptive deme formation fecundity and population growth rates26. This is apparent is genetic isolation among insects despite their proximity. when phenotypic variation in plant traits such as nutritional Hence most experiments testing the hypothesis have emquality and/or chemical defense leads to differential herployed relatively non-dispersive organisms such as scale bivory, a conspicuous feature in many natural plant popuinsects, and these studies are about evenly divided in suplations including Rhus27, Salix28, Populus29 and Quercus30. porWJ5J6 and rejection33J4J7 of the hypothesis (Table 1). Variation among trees in quality, natural enemy distribution, Even minimal gene exchange can prevent the evolution of and herbivore social interactions probably produced treelevel genetic structure in willow leaf beetle populationGJ2. locally adapted demes. Hanks and Denno detected local adap tation in the highly sessile armored scale only when the host Extreme differential herbivory inspired the adaptive mulberry trees were isolated by more than 300 m (Ref. 35). deme formation hypothesis25, which predicts that insects However, gene flow per se is a poor predictor of deme forquickly adapt to the phenotypic traits of individual host mation. Three studies examined deme formation in dispersive plants. The theory predicts that as insects repeatedly coloninsect&BJg, and two reported adaptive genetic variation at ize the natal host, they become more successful at exploiting the spatial scale of individual host plantslOJ8.In the disperit and less successful at exploiting novel conspecific plants. After several generations, natural selection produces fine- siveSti/bosis quadricustatella leafminer population, adaptive Table 1. Experimental tests of the adaptive deme formation hypothesis
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REVIEWS variation occurred on experimental trees growing from lo-150m apartlo. A recent field experiment suggests that adult .S.quadricustutefIa females selectively oviposit on particular Quercus geminata trees, which may contribute to reproductive isolation in this dispersive insectso. Direct estimates of gene flow (reviewed by Peterson and Denno2) further illustrate that dispersal abilities alone do not determine the magnitude of isolation among individuals in a population. lntrapopulation genetic isolation and structure, despite high potential gene flow may necessitate correlations between genes promoting physiological adaptations and genes promoting reproductive isolation, via mechanisms such as pleiotropy or linkage 1,40.Estimates of gene flow, in conjunction with the deme formation experiments, indicate that strong selection pressures can and do counteract the effects of gene exchange, even across very narrow spatial boundaries. Agents of selection and adaptive deme formation Host plants If genetic structure appears among organisms in close proximity, what selection forces lead to it? According to the deme formation hypothesis, insects adapt to the phenotypic traits of individual trees25. A fundamental assumption of the theory is that insects inhabiting natal plants suffer less mortality from plant defense mechanisms than insects colonizing novel plants. Despite its importance to our understanding of adaptive evolution, only two studies have explicitly examined plant impacts on insect performance in the context of selection and deme formationlOJ8. Determining the cause of insect mortality can be difficult, particularly for those species that feed externally. On the other hand, endophagous insects -those that feed and reside within host-plant tissues -reveal clues about their fate. Mopper et al.10examined plant-mediated mortality among S. quadricusfate/la leafminers (Fig. 1) transferred to natal and novel sites, natal and novel host species (Q. geminatu and Q. myrtifoliu), and natal and novel Q. geminutu trees within a site. Consistent with the deme formation hypothesis, they discovered significantly reduced plant-mediated mortality in the natal treatment groups at each of the three spatial scales. Thus, although adult .S. quudricustutellu are dispersive, leafminers may adapt to individual host plants despite the potential for gene exchange among trees. Allozyme studies are currently under way to further explore genetic structure in the leafminer-oak system (K. Landau and S. Mopper, unpublished data). Stiling and Rossi also examined agents of selection in their test of the adaptive deme formation hypothesis. They presented natal and novel plants of sea oxeye daisy (Borrichiu frutescens) to ovipositing females of a gall-forming midge, Asphondyliu borrichiu and observed that gall size was significantly larger on natal plants, and adult flies preferred natal to novel plants for oviposition. Natural enemies In S. quudricustutellu leafminers, parasitism and predation can be identified by characteristic scars on the leaf. Despite reduced plant-mediated mortality on natal trees, rates of leafminer survival were similar on natal and novel treeslo. This resulted from a corresponding increase in naturalenemy mortality of leafminers inhabiting natal trees. In effect, plant- and enemy-mediated mortality were balanced such that total leafminer mortality was similar on natal and novel trees. This intriguing result suggests that natural enemies as well as their phytophagous prey may be locally adapted at TREE vol.
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the tree spatial scale. Are endophagous insects such as leafminers and gallformers more apparent to natural enemies on natal than on novel host plants? Perhaps natal inhabitants harbor superior physiological adaptations that result in more rapid growth than recent colonizers of the same plant. Faster growth may produce mines that are more conspicuous to enemies. Alternatively, natal herbivores may metabolize and excrete phytochemicals more efficiently, thereby increasing their conspicuousness to natural enemies, such as hymenopteran predators and parasitoids, which rely on chemical cues to locate prey. Implications of adaptive deme formation One discovery of the deme formation experiments and other studies of population genetic structure is that dispersal ability is a poor predictor of genetic isolation2. Highly dispersive insects can exhibit greater local adaptation than sessile insects (Table 1). These inconsistencies may be explained in part by mode of feedinglOJ8.Endophagous insects such as leafminers and gallformers are intimately associated with their host because they are confined to the same plant tissue throughout larval development. Such intimacy may magnify the selection pressures imposed by host plants and natural enemies to a degree not experienced by externallyfeeding herbivores”). Only by identifying agents of selection and mechanisms of reproductive isolation, can we understand fine-scale adaptive evolution. Long-term field experiments that identify sources of mortality are critical because insect densities, natural enemy populations, and host-plant quality can vary widely between yearsso. The field experiments should be combined with measures of gene flow and allele frequencies within and among discrete demes. Natural undisturbed insect and plant populations are often structured into discrete demes or patcheslz. Yet there has been virtually no research investigating how genetic structure in plant populations impacts genetic structure in insect populations41. Understanding the mechanisms promoting and preventing population genetic heterogeneity is important for both applied and basic science. One of the most pressing conservation issues today is the maintenance of genetic variation in rapidly shrinking natural plant and animal populations. The reduction of individual genetic variation can have devastating consequences for the entire population. The deme formation experiments described herein indicate that phytophagous insects in heterogeneous plant pop& lations are less able to exploit non-natal plants, thereby reducing the possibility of widespread contagion and insect , obtbreaksl2. Presumably, phytophagous insects can more rapidly exploit entire plant populations composed of genetically similar individuals. In a natural population of pinyon pine (Pinus e&/is), chronic insect herbivory reduced plant growth and reproduction, and was most severe for trees that were homozygous at two enzyme loci42. Without substantial genetic Fig. 1. Two active Stilbosis qua&ivariation, recombination and custatella leafminer larvae in a water oak (Quercus nigra) leaf. This photo outcrossing may not be suffigraph illustrates the intimate associcient to increase plant resistation between endophagous insects ance to adapted herbivore+u. and their plant hosts. Understanding how natural selection, gene flow and isolating I 237
REVIEWS mechanisms operate at fine-scales provides valuable insight into how evolution operates at the species level and beyond.
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Acknowledgements I thank Merrill Peterson, Peter Stiling, Sharon Strauss and two anonymous reviewers for their insightful comments on the manuscript. This research was supported by USA grants NSF BSR90-07144, EPSCoR NSF/LEQSF(19921996)-ADP-02
and LEQSF(1994-1996)-RD-A-37.
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