John Poulsen

Evolution of Host Specialization by Insects

Anstett, M.C., Hossaert-McKey, M. and Kjellberg, F. Figs and fig pollinators: evolutionary conflicts in a coevolved mutualism. Trends in Ecology and Evolution 12(3), 94-99. Anstett et al. question why conflicts between mutualists do not destabilize interactions. Using figs and wasps as an example, they conclude that organisms must first have the right preadaptation allowing them to respond to selection in a manner than maintains the mutualism.

Bass, M. and Cherrett, J.M. 1994. The role of leaf-cutting ant workers (Hymenoptera: Formicidae) in fungus garden maintenance. Ecological Entomology 19: 215-220. This article is essentially a background paper describing the management of fungal gardens by ants. Ants gain enzymes to help break down plant tissue for food while regulating hyphal growth and controlling the growth of contaminant fungi.

Berenbaum, M.R. and Passoa, S. 1999. Generic phylogeny of North American Depressariinae (Lepidoptera: Elachistidae) and hypotheses about coevolution. Annals of the Entomological Society of America 92(6): 971-986. Berenbaum and Passoa constructed a phylogeny of Depressariinae using morphological characters to determine if it adapted to its host, wild parsnip, via reciprocal selection. Host shifts between unrelated host plant families and reversions to host plant groups were abundant; and association with plants in Apiaceae and Asteraceae led to rapid speciation. One wonders how all these results can come from an article that provides a single tree without any statistics or comparison to a null model.

Bernays, E. and Graham, M. 1988. On the evolution of host specificity in phytophagous arthropods. Ecology 69(4): 886-892. Bernays and Graham argue that chemical coevolution between plants and herbivores has been overemphasized, and suggest that predators and parasites drive the evolution of specialized host ranges in phytophagous insects. Other factors beyond plant chemistry should be considered as determinants of host specificity, but the authors overstate predation as an evolutionary force.

Currie, C.R., Scott, J.A., Summerbell, R.C., and Malloch, D. 1999. Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 398, 701- 714. Currie et al. report that Attini ants that maintain specialized fungal gardens also carry a filamentous bacterium that produces antibiotics specifically targeted to suppress the growth of the specialized garden-parasite Escovopsis. This article provides demonstrates that mutualisms and coevolution may be complex and multi-tiered.

Dobler, S., Mardulyn, P., Pasteels, J.M., and Martine, R.R. 1996. Host-plant switches and the evolution of chemical defenses and life history in the leaf beetle genus Oreina. Evolution 50(6): 2373-2386. Oreina beetles appear to be more flexible in defense mechanisms, reproduction, and reliance on host plants than other beetles. Dobler et al. use cladistic analysis to estimate a phylogeny, and hypothesize that ecological traits, like autogenous defense and mobile externally feeding larvae, allowed these beetles to switch host plants readily. These results contrast to with those on Ophraella beetles that have a limited number of possible host plants due to genetic constraints (Futuyma et al. 1993).

Erlich, P.R., and Raven, P.H. 1967. Butterflies and plants: a study in coevolution. Evolution 18:586-608. Erlich and Raven’s paper is a classic and mentioned in nearly all the other studies cited here. They argue that the host-plant associations we see today have been shaped by a stepwise coevolutionary process in which plants evolve defenses against natural enemies, and these enemies in turn evolve new capacities to cope with these defenses.

Farrell, B.D. and Mitter, C. The timing of insect/plant diversification: Might Tetraopes (Coleoptera: Cerambycidae and Asclepias (Asclepiadaceae) have co-evolved? Biological Journal of the Linnean Society 63(4): 553-577. Farrell and Mitter reject host-tracking between beetles and their hosts, and find the opportunity for coevolution in the history of the association. They used a phylogeny based on morphology and allozymes, which was supported by fossils and biogeography. More molecular characters need to be analyzed, but the authors don’t overstate their results.

Futuyma, D.J., Keese, M.C., and Scheffer, S.J. 1993. Genetic constraints and the phylogeny of insect-plant associations: responses of Ophraella Communa (Coleoptera: Chrysomelidae) to host plants of its congeners. Evolution 47(3): 888-905. Futuyma et al. found evidence for genetic variation in feeding responses of five of seven test species. Comparing the results of feeding experiments to an Ophraella phylogeny, the genetic variation proved to be adapted for plants O. communa does not use as a host, rather than historical hosts. Both ecological and genetic variation and constraints may guide host affiliation.

Futuyma, D., Keese, M.C., and Funk, D.J. 1995. Genetic Constraints on Macroevolution: The Evolution of Host Affiliation in the Leaf Beetle Genus Ophraella. Evolution 49(5), 797-809. Futuyma et al. test the hypothesis that the evolution of associations of phytophagous insects on host plants are influenced by limitations on genetic variation. Genetic constraints were found to constrain or at least bias the evolution of host associations. This paper requires a thorough reading, and, with the exception of adding more Ophraella species, is not very different from their 1993 article (see above).

Funk, D.J, Futuyma, D.J., Orti, G., and Meyer, A. 1995. A History of Host Associations and Evolutionary Diversification for Ophraella (Coleoptera: Chrysomelidae): New Evidence from Mitochondrial DNA. Evolution 49(5), 1008-1017.

Funk et al. update their old estimate of Ophraella phylogeny with a new tree based. The phylogeny suggests that diversification of Ophraella likely occurred as host shifts rather than cospeciation between insects and their hosts. This paper is a good example of the role of phylogenetic trees in interpreting relationships between hosts and insects.

Gaume, L. and McKey, D. 1999. An ant-plant mutualism and its host-specific parasite: activity rhythms, young leaf patrolling, and effects on herbivores of two specialist plant-ants inhabiting the same myrmecophyte. Oikos 84: 130-144. Two ant species inhabit the same tree host; one ant acts as a mutualist, the other a parasite. Differences in ant behavior are reported and hypotheses are stated to explain the evolution of these relationships and the co-existence of a parasite and a mutualist on the same host population. The hypotheses are speculative and need further testing by the authors, and phylogeny may resolve the relationships of the ants with their host plant..

Herre, E.A., Knowlton, N., Mueller, U.G., and Rehner, S.A. 1999. The evolution of mutualisms: exploring the paths between conflict and cooperation. Trends in Ecology and Evolution 14(2), 49-53. This review heralds molecular techniques as analyses that will transform our knowledge of mutualisms. The authors suggest that further research be aimed at determining general principles of mutualisms and quantifying the costs and benefits to each party to determine what factors maintain the alignment of interests. These ideas are prevalent throughout the literature, and it is not obvious that this review makes a contribution to the field.

Janz, N. and Nylin, S. 1998. Butterflies and plants: A phylogenetic study. Evolution 51(2): 486-502. Using a butterfly phylogeny, Janz and Nylin focus on the patterns and determinants of host shifts. They find that host shifts are most common between closely related species and hypothesize that constraints on genetic variation, host-plant chemistry, or habitat and community structure play a role in shaping butterfly-host associations.

Keese, M.C. 1997. Does escape to enemy-free space explain host specialization in two closely related leaf-feeding beetles (Coleoptera: Chrysomelidae)? Oecologia 112: 81-86. The ever-studied Ophraella beetles were manipulated on host plants to test whether the hypothesized shift from an ancestral host Ambrosia to the natural host Iva was caused by a move to enemy-free space. The author estimated egg predation, successful egg hatch, and larval parasitism, but found little evidence that escape to enemy-free space maintains the monophagy of O. notulata. It is good to see that both genetic and ecological explanations of host specialization are being tested.

Knowles, L.L., Levy, A. McNellis, J.M., Greene, K.P., and Futuyma, D.J. 1999a. Tests of Inbreeding Effects on Host-Shift Potential in the Phytophagous Beetle Ophraella Communa. Evolution 53(2): 561-567. Knowles et al. determined that inbred lines of beetles did not have increased phenotypic variance within the lineage, discounting the idea that host shifts in this beetle evolved by peak shifts in bottlenecked populations. This article is a continuation of the work on Ophraella beetles and supports the results of Knowles (1999b) that population bottlenecks likely did not attribute to host shifts.

Knowles, L.L., Futuyma, D.J., Eanes, W.F., and Rannala, B. 1999b. Insight into Speciation from Historical Demography in the Phytophagous Beetle Genus Ophraella. Evolution 53(6), 1846-1856. Knowles et al. analyzed mitochondrial cytochrome oxidase I sequences to reconstruct the historical demography of Ophraella communa. Results suggest that O. bilineata arose from an O communa-like ancestor by allopatric speciation with rapid isolation in a geographically restricted area.

Norton, D.A. and Carpenter, M.A. 1998. Mistletoes as parasites: host specificity and speciation. Trends in Ecology and Evolution 13(3), 101-105. Norton and Carpenter offers a good review of the theories of host-parasite speciation through cospeciation or host switching. Advances in our understanding of host specificity and speciation patterns are applied to mistletoes.

North, R.D., Jackson, C.W., and Howse, P.E. Evolutionary aspects of ant-fungus interactions in leaf-cutting ants. Trends in Ecology and Evolution 12(10): 386-388. North et al. review the host-parasite relationship between Attini ants and fungi. This paper explains the nature of the association in the context of phylogeny and outlines the interactions between the ants and fungus from foraging to the final product.

Page, R.D.M. and M.A. Charleston. 1998. Trees within trees: phylogeny and historical associations. Trends in Ecology and Evolution 13(9), 356-359. Page and Charleston argue that associations between genes and organisms, organisms and organisms, and organisms and areas are parallel problems. The strength of this article is that it tries to define a common vocabulary and unify the disparate disciplines of molecular systematics, parasitology, and biogeography on the grounds that they can employ the same analytical tools.

Paterson, A. and Gray, R. 1997. Host-parasite co-speciation, host switching, and missing the boat. In Host-Parasite Evolution: General Principles and Avian Models. Clayton, D.H. and Moore, J. (eds.). Oxford University Press, Oxford: 236-250. The authors postulate three steps required to test host-parasite co-speciation: 1) construction of accurate trees for both hosts and parasites, 2) comparison of phylogenies with quantitative methods, 3) testing whether congruence between host and parasite populations are greater than expected by chance. If all studies of host-parasite evolution rigorously applied the above procedures (and the authors point out that very few studies do), the results would be much more robust.

Renaud, F., Clayton, D., and De Meeus, T. 1996. Biodiversity and evolution in host-parasite associations. Biodiversity and Conservation 5: 963-974. More ideas concerning host-parasite evolution, but not specifically host specialization. Renaud et al. review host-parasite relationships in the context of game theory, demonstrating that there are a diversity of host-parasite associations largely determined by the evolution of a host’s resistance and a parasite’s virulence. Not surprisingly, the author concludes that ecologists and geneticists need to collaborate to further examine relationships, which govern the evolutionary ecology of parasitism.

Thompson, J.N. 1999. The Evolution of Species Interactions. Science 284, 2116-2118.

Thompson’s review emphasizes that interactions between species are evolutionary malleable and affect species diversification. Interactions are likely to be in continual flux as they evolve in different ways between populations, across geographic gradients, and between selection mosaics. This article is a reminder that host specialization is an ongoing process.

Wetterer, J.K., Schultz, T.R. and Meier, R. 1998. Phylogeny of fungus-growing ants (Tribe Attini) based on mtDNA sequence and morphology. Molecular phylogenetics and evolution 9(1): 42-47. Wetterer et al. examined the phylogenetic relationships among the fungus-growing ants using parsimony analysis of molecular and morphological data. One results of the analysis is that yeast-growing species were determined to be derived rather than the primitive condition. The authors used a limited subset of ant species and don’t say much else in the article, besides presenting the phylogeny.

Yamamura, N. 1996. Evolution of mutualistic symbiosis: A differentiated equation model. Researches on Population Ecology 38(2): 211-218. Yamamura presents a series of differential equations created to identify the conditions for the evolution of mutualism from parasitism. Vertical transmission rate (transfer of parasites from generation to generation of hosts) is the most important factor for reduction of parasite virulence. Initiation of the one-way evolutionary process from parasitism to mutualism may occur when the parasite wins the conflict against the host in the vertical transmission rate.