Coevolution: Evolutionary Interactions Between Herbivorous Insects and Plants

1. Coevolution: Evolutionary Interactions Between Herbivorous Insects and Plants Peter B. McEvoy Ent 420/520 Insect Ecology

2. Questions (Futyma and Slatkin 1983) • Adaptive Radiation.How often has the adaptive radiation of a group depended on radiation of other groups with which they interact? • Speciation.Does speciation of hosts and parasite often occur in parallel? • Defense.Do defense systems of prey become more complex over evolutionary time with addition of new defenses to the armory, or are old defenses traded in for new ones? • Specialization, Virulence-resistance.Do parasites tend toward specialization or toward benign or even mutualistic relationship with their hosts? • Nature and power of historical explanation.In general, how much of the history of evolution must be explained in terms of the evolutionary effects of interspecific interactions?

3. Evolution of Insect-plant Relationships • Plant effects on insects.Do plants exert selection pressure on the insects? • Insect effects on plants.Do insects exert selection pressure on the plants? • Symmetry.Are the selective interactions between insects and plant reciprocal? • Do related insects feed on related hosts? • Is specialization an evolutionary dead end?

4. Alternative Theories on Herbivore-Plant Evolution • Coevolution (Ehrlich and Raven 1964) • Diffuse Coevolution, Community Coevolution (Fox 1988) • Geographic Mosaic Theory of Coevolution (Thompson 1994, 2005) • Sequential Evolution (Jermy 1976, 1984, 1991)

5. Escape and Radiation Coevolution Hypothesis (Ehrlich and Raven) Many factors influence the evolution of herbivorous diets, but plant chemistry is central • Secondary chemicals produced by chance and modified under selective pressure from herbivores • Plant escape and radiation: chemically-defended plants escape herbivores and radiate • Insect escape and radiation: counter-adaptations by insects allow insects to overcome host defenses, exploit previously defended hosts, escape competition from other insects, and radiate • Parallel diversification in insects and plants: Insects and plants augment one another’s diversity through coevolution, reciprocal evolutionary change in interacting species

6. Critique of Coevolution (Schoonhoven et al. 1998) • Allelochemicals. Same secondary plant compound may have different functions in different insects – toxic, deterrent, attractant; negative, neutral, positive • Plant defense and radiation. Little evidence that plants have evolved defenses under herbivore selective pressure or that such plants could diversify more effectively because they were defended • Insect offense and radiation. Processes of speciation currently known do not support hypothesized radiation since interspecific competition generally weak • Reciprocal speciation rarely found except in pollinators and plants, microbial symbionts and their hosts. Related insects often feed on unrelated hosts.

7. No single factor drives insects to specialize • Escape from interspecific competition • Reduced exposure to predators (enemy escape) • Increased efficiency at detoxifying plant allelochemicals • Genetically based trade-offs in offspring performance • Increased efficiency in host finding

8. No clear link between chemistry and speciation • Spatial barriers • Behavioral barriers • Asynchrony in life history • Hybrid incompatibility Speciation Reproductive isolation Chemistry

9. Asynchrony in Emergence of Three Apple Maggot RacesChanges in preference and performance conserved by temporal separation of host races and assortative mating

10. Oviposition Preferences of Euphydryaseditha Changedas ancestral host decreased and novel host increased Novel Host increased Ancestral Host decreased

11. Geographic Mosaic Theory (Thompson) recognizes the importance of spatial heterogeneity and movementWhy retain the concept of “coevolution”? • Local variation in environment and population and community structure • Local variation in outcome of interactions and specialization • Balance between gene flow and selection • Results in a shifting, geographic mosaic of interaction that need not result in a simple escalation of adaptations and counter-adaptations

12. Sequential or Asymmetrical Evolution Theory (Jermy) • Sequence of events. Evolution of insects follows the evolution of plants without significantly affecting plant evolution • Interaction strength. Plants exert strong selective pressure on insects, whereas reciprocal negative effect of insects on plants is rare and weak • Speciation in insects may be mediated by plants, but speciation in plants unrelated to insects • Origin of plant traits. Switches in host occur, but no evidence that acquisition of new host has changed the traits of a plant

13. Tree of Plants ucjeps.berkeley.edu/TreeofLife/hyperbolic.php

14. Potential resources Increased stature – up-standing plants  overtopping  trees Appearance of Vasculature (Cordaites) Appearance of seeds (spores terminal sporangia terminal spike heterosporous condition seeds) Leaves – microphylls  megaphylls  laminate leaves  insect damaged leaves Flowers and fruits Species - diversification of Angiosperms toward end of early Cretaceous Modes of exploitation -Sucking probably earliest mode of feeding, followed by chewing, while mining and galling appear much later Chronology of Plant and Insect Evolution (Smart and Hughes 1972)

15. More Plant Species  More Insects Species Higher Plant Species Diversity  More Insects Species

16. More Plant Architectural Diversity  More Insect Species Number of phytophage species S increases with area of host For a given host area, the number of phytophage species increases with the architectural diversity of the host plant (e.g. we find progressively fewer phytophages on trees, shrubs, herbs)

17. Diversities of Fossil Families Within Insect Orders of Phanerozoic (Labandeira et al 1993) Angiosperms appear ~2/3 of the way up the band of Mesozoic, radiate extensively in Cenozoic (Tertiary) Possibly accelerated Hym, Lep, Dip, Col No such effect on Orthop, Homop, Heterop Insect diversification depends on intrinsic trends rather than environmental (ecological) conditions

18. Insect Familial Diversity From Triassic to Present Overall, appearance and ascendancy of the angiosperms associated with a slow-down rather than an acceleration of insect familial diversification Caveat: family diversification not necessarily identical with species diversification

19. Summary From Fossil Evidence • Timing of events.No precise coincidence in time between evolution of higher plants and insect taxa.Hymenoptera, Lepidoptera,Diptera, Coleoptera radiationsmay have accelerated with appearance and radiation of angiosperms • Expanding resources.An increase in plant structural and architectural diversity, plant taxonomic diversity, opens up new possibilities for insect diversification.

20. Phylogenetic Evidence • Host records - field and literature surveys • Phylogenies (plant and insect) are constructed based on morphological, secondary chemical, molecular, and other characters • Patterns - inferences about the predictability and stability of the host range • Pattern 1: Taxonomically related insects feed on taxonomically related hosts • Pattern 2: Parallel evolution of insects and plants (Coevolution) • Pattern 3: Non-Parallel evolution of insects and plants

21. Phylogenetic Patterns 2:Parallel evolution of insects and plants (Coevolution)

22. Phylogenetic patterns 3: Non-Parallel evolution of insects and plants

23. Phylogenetic AnalysisSample of25 insect-plant associations (Mitter and Farrell 1991, Farrell et al. 1992, Farrell and Mitter 1993, Futuyma and Mitter 1997) • Taxonomic similarity. Shifts among plant families are relatively rare, but shifts within plant families are relatively common • Ancient origin. Conservative plant-insect associations are probably very old, from about 70 to 100 million years old • Seldom evolve by strict coevolution. The exception, rather than the rule, is finding close concordance in insect and plant phylogenies matching different insect species with different plant species in a tight coevolutionary relation, but broad concordance is found higher in the taxonomic hierarchy • Similar hosts in different regions. Similar host ranges are revealed by comparing related insects in different biogeographic regions, another indication that that diets are phylogenetically conservative • Chemical similarity. Some host ranges are conservative with respect to phytochemistry

24. Challenges to Conventional Wisdom • Phylogenetically conserved mechanisms. Host use is not necessarily “phylogenetically conservative” – taxonomically related insects may feed on taxonomically unrelated plants • Origins and Potentials of specialists. Specialization is not necessarily “derived” – both primitive and derived taxa may specialize, and specialization need not be “an evolutionary dead end”

25. Plant coumarins, Swallowtails, and Other Insects An Example of a Coevolved System (Berenbaum) • Diet phylogenies of several herbivore clades using taxonomically disparate hosts may be interpretable as conserved associations with coumarin-bearing plants • Escalation of defense • Radiation of plants • Radiation of insects

26. Parsnip Moth Depressaria pastinacella Parsnip Moth Depressaria pastinacella Heracleum sphondylium

27. Coumarins Vary From Simple to Complexin Escalating Plant Defense 30 plant families 8 plant families 2 plant families Fabaceae (2) Apiaceae (11)

28. PLANT DIVERSITY:More Extensive Radiation by Plants With More Complex furanocoumarins

29. INSECT DIVERSITY: More Extensive Radiation in Insects Associated With Plants Having More Complex Coumarins

30. Greater Degree of Specialization Among Insects Feeding on Plants With More Complex Coumarins

31. Genetics • Genetic basis for chemical variation among individual wild parsnip plants Pastinaca sativa attacked by the parsnip webworm Depressaria pastinacella (Oecophoridae) • Nature of inheritance for plant resistance.Quantitative and polygenic resistance • Negative correlations in resistance traits of the plant.Negative correlation between two traits (bergapten and sphondin) conveying resistance limits resistance in the plant population when herbivore present • Costs of defense for plant.Negative correlation between several resistance factors and total seed production in greenhouse where herbivore is absent. • Lingering Questions:Are there similar genetic constraints on response of insect to selection by plant chemistry? Polygenic control of resistance-breaking ability? Negative correlations in traits conferring resistance breaking ability?

32. Overall Summary • Adapative hurdles.Feeding on plants presents formidable hurdles to insects, but once hurdles are cleared, radiation may be dramatic • Coevolution.Evolutionary interactions between insects and plants have been described as coevolution, but strict reciprocity has not been demonstrated for any complex of plants and herbivores. This has spawned alternative theories. • Coevolution is more likely to occur when an insect has few host species and its hosts harbor few natural enemies.

33. Parsnip – Webworm interaction Pastinaca sativa or parsnip introduced to NA almost 400 yrs ago Heracleum lanatum or cow parsnip is an alternate host Parsnip Pastinaca sativa Heracleum sphondylium Parsnip Moth Depressaria pastinacella reassociated with parsnip in mid 19th century Larvae attack seeds CalPhotos

34. Geographic Mosaic Hypothesis(Thompson 1994, 1999, 2005) • Outcomes of interspecific interactions can vary among populations due to structural differences in the communities in which interactions are embedded • Where selection intensity is great, reciprocal responses are likely in so-called “hotspots” • In contrast, where selection pressures are relaxed, reciprocal responses in “coldspots” are far less likely to occur

35. Geographic Variation in Outcomes has been Reported for… • Plants and Pathogens • Hosts and Parasites • Hosts and Parasitoids • Competitors • Pollinators or floral parasites and plants • Herbivores and plants Coevolutionary changes in chemical defense have rarely been examined in this context

36. Department of EntomologyUniversity of Illinois May R. Berenbaum Arthur R. Zangerl

38. A Model System • Plate 1. Clockwise from left: wild parsnip damaged by parsnip webworm in The Netherlands, parsnip webworm in the United States, and prepupal parsnip webworm parasitized by Copidosoma sosares in The Netherlands. Photo credits: A. ZangerlCopidosoma Sosares (Walker) (Hymenoptera: Encyrtidae)

39. Evidence of hot spots and cold spotsPhenotype matching between plant furanocoumarin profile and insect detoxification profile • Credentials of the sample. Four populations of webworms and wild parsnips in the midwestern United States • Operational definitions of resistance and virulence. Evaluated correspondence between resistance in the wild parsnip populations (capacity to produce furanocoumarins) with “virulence” (capacity to detoxify furanocoumarins) in each webworm population • Resistance factors. Four furanocoumarins known to influence the interaction between webworms and parsnips - bergapten, isopimpinellin, xanthotoxin, and sphondin—were quantified in the seeds of wild parsnips and, as well, rates of metabolism of these four furanocoumarins were quantified in the associated insect populations

40. How does interaction strength vary with community structure? • Interaction with natural enemies and alternative host plants can reduce the intensity of coevolutionary interaction between webworms and parsnips • Many of the models of coevolutionary dynamics are based on two-species interactions and relatively few empirical studies involve multispecies interactions Restated diagrammatically as follows…

41. Expected Effects of Varying Community Structure Parasitoid Herbivore Plant Plant Coevolutionary ‘Temperature’: Expectation: --- Cold Spots --- Hot Spot H-P Well-Matched H-P Mismatched

42. Hypotheses • Outcomes of interaction between the wild parsnip and the parsnip webworm, compared at home (area of indigeneity) and abroad (area of introduction) • If webworms act as selective agents on furanocoumarin content of hosts, they will likely • Avoid or fail to utilize plants with furanocoumarin profiles that confer resistance • Thrive on plants with furanocoumarin profiles that are insufficient to confer resistance. • The selective impact of the parsnip webworm on the wild parsnip is likely reduced by • alternate, chemically different host plants • a specialist parasitoid natural enemy that inflicts significant mortality Leading to an absence of a predictive relationship between webworm presence and host plant chemical composition

43. Methods • Pastinaca sativa and Heracleum spp. surveyed in Europe during only one year 2003 – ignorestemporal variation (within and between years) at each location – i.e. sample long on space, short on time • Counted parasitized and unparasitized webworms – with what probability of detection? • Strength of interactions – ‘interaction temperature’ classified as categorical variable, cold or hot, depending on whether webworms were prevalent or rare – a cursory measure of interaction strength • Webworms collected to test detoxification capacity • Five furanocoumarins measured in seeds of P. sativa collected in USA and EU in 2004 (damage also recorded). Compared furanocoumarin seed concentrations as a function of continent and interaction temperature. • In Europe 4 of 14 (~30%)populations were cold and in the United States, 3 of 9 (33%) populations were cold – so frequency of hot and cold sites similar between continents

44. Results to be examined • Surveys of webworms and parasitoids in European populations of P. sativa and H. sphondylium • Furanocoumarin detoxification capacity of European and midwestern U.S. populations of parsnip webworms • Differences in seed furanocoumarin content between European host plants • Evidence for selection by webworms on furanocoumarin chemistry of European host plants • Differences betweenhot and cold regions within continents and not between continents in seed furanocoumarin content

45. Surveys of webworms in EU hot • Parsnip webworm infestation levels in European populations generally higher for Heracleum sphondylium (black circles) than Pastinaca sativa (gray circles) in 2003 cold Surveys of parasitoids less conclusive

46. Detoxification ability of webworms lower at home (Neth) than abroad (Midw) % indicate magnitudes of differences • Fig. 4. Least-square means and standard errors of furanocoumarin detoxification rates for midwestern U.S. and Netherlands populations of parsnip webworms. Percentages above bars indicate magnitudes of significant differences between continents based on a mixed/nested ANOVA (continent was a fixed effect, and population was a random effect nested within continent). For imperatorin, bergapten, isopimpinellin, xanthotoxin, and sphondin, P values for the main effect of continent were 0.004, 0.031, 0.049, 0.021, and 0.033, respectively

47. Chemical profiles differ on two hosts in Europe % indicate magnitudes of differences • Fig. 5. Least-square means and standard errors of seed furanocoumarin content of Heracleum sphondylium and Pastinaca sativa in Europe. Percentages above bars indicate magnitudes of significant differences between species based on a mixed/nested ANOVA (species was a fixed effect, and population was a random effect nested within species). For imperatorin, bergapten, isopimpinellin, and xanthotoxin, P values for the main effect of species were <0.001, 0.012, 0.008, 0.021, and <0.0013, respectively. Tests were not conducted for sphondin, which was not detected (n.d.) in H. sphondylium, or for angelicin, which was not detected in P. sativa

48. Evidence of Selection by Webworms on furanocoumarin chemistry in EU hosts is spotty • Three under selection: 3 of 11 populations show evidence of selection • Two hot, one cold. 2 of these 3 had high webworm infestations (54% and 56% of plants attacked), the other low (8.9%) • Match within one. In 1 of the 2, plants free of webworms had higher xanthotoxin • Match within other. In the other, plants without webworm damage had higher imperatorin, isopimpinellin, and sphondin content

49. Difference in furanocouarin content between hot and cold regions within continents, but not between continents % indicate magnitudes of differences • Fig. 6. Least-square means and standard errors of seed furanocoumarin concentration for wild parsnips as a function of prevalence of webworms (interaction temperature: webworms are rare in cold regions and common in hot regions). Percentages above bars indicate magnitudes of significant differences between hot and cold regions based on a mixed/nested ANOVA (continent and interaction temperature were fixed effects, and population was a random effect nested within the main effects) Continent and Hot/Cold interact in case of sphondin

50. Conclusions • Home and Away Populations Similar. Patterns are more reflective of interaction temperature than of continental origin • Introduced System is Simplified. The ubiquitous two-species interaction in North America is in fact exceptional in Europe: webworms could more reliably be found infesting H. sphondylium even where P. sativa was available as well. • Interactions among three trophic levels. A preference for H. sphondylium exists despite the comparatively high probability of parasitism associated with this host plant and may reflect the overall lower furanocoumarin content of H. sphondylium