ANNOTATED BIBLIOGRAPHY

Ecology and Phylogeny in the Coevolution

of Pollinator-Plant Systems

Melissa R. Andres

GENERAL

Janzen, Daniel H. 1980. When is it coevolution? Evolution 34(3): 611-612.

Calls attention to the misuse of the concept of "coevolution". Redefines it as: "… an evolutionary change in a trait of the individuals in one population in response to a trait of the individuals of a second population, followed by an evolutionary response by the second population to the change in the first." Coevolved organisms must have this reciprocal interaction over evolutionary time. Janzen's attempt to clarify Ehrlich and Raven's (1964) terminology.

Feinsinger, Peter. 1983. Coevolution and pollination. In Coevolution (D.J. Futuyma and M. Slatkin, Eds.). Sinauer Associates, Inc. Massachusetts: Sunderland.

A fascinating and very readable chapter focusing on the community ecology of coevolution between plants and their pollinators. Tries to get at the question of when coevolution will occur. Examines the likelihood of specialization from the plant's perspective (how well will a certain pollinator transfer pollen from one individual plant to another of the same species?), as well as the pollinator's perspective (does this plant offer adequate rewards at a low cost of energy?). Examines three (non-obligate) examples: (1) Euglossine bees and orchids, (2) bumblebees and bee-flowers, and (3) hummingbirds and hummingbird-flowers. Asks what the chances of reciprocal evolution would be in each of these cases.

Keister, A.R., Lande, R., and Schemske, D.W. 1984. Models of coevolution and speciation in plants and their pollinators. The American Naturalist 124(2): 220-243.

This is the population biologist's look at the coevolution of plants and their pollinators. These authors build mathematical models to evaluate the roles of population structure and sexual selection in determining the chance of coevolution and rate of speciation between plants and their pollinators. Asks what factors will affect the stability of a coevolutionary relationship? Discuss three examples: (1) orchids and orchid bees, (2) figs and fig wasps, and (3) yuccas and yucca moths.

Ollerton, J. 1996. Reconciling ecological processes with phylogenetic patterns: the apparent paradox of plant-pollinator systems. Journal of Ecology 84: 767-769.

Points out an apparent paradox: If most pollinators are generalists, and most angiosperms are generalists in their pollinator requirements, how could directional selection in flowering plants occur? Proposes four possible resolutions. A quick and insightful read.

Waser, Nickolas M. 1998. Pollination, angiosperm speciation, and the nature of species boundaries. Oikos 81: 198-201.

Brings the commonly accepted view that pollinators significantly contribute to the speciation of flowering plants under scrutiny. While this is commonly assumed, very little experimental evidence has been produced. Suggests that floral reproductive isolation via pollinators unlikely. Proposes a few lines of research needing exploration in order to address this issue. An easy read.

DIFFUSE MUTUALISMS OF POLLINATORS

Jordano, Pedro. 1987. Patterns of mutualistic interactions in pollination and seed dispersal: connectance, dependence asymmetries, and coevolution. The American Naturalist 129(5): 657-677.

Builds on the view that most pollinator (and seed disperser) systems are comprised of generalists. Examines communities of "diffuse mutualists" in a food web context in order to calculate connectance and strength of interaction values as the number of species involved in the mutualism increases. This is a really interesting paper, but a little hard to read.

Memmott, Jane. 1999. The structure of a plant-pollinator food web. Ecology Letters 2: 276-280.

This short and sweet summary vividly reveals the lack of specialization typically found in plant-pollinator interactions. Generalization is common: Pollinators usually attend a range of host plants, and plants usually host a range of pollinators. The real goal of this paper is to stimulate the use of methods of food web construction and analysis in plant-pollinator studies.

SPECIALIZED MUTUALISMS: The Classic Examples

The Fig - Fig wasp system

Weibes, J.T. 1979. Co-evolution of figs and their insect pollinators. Annual Review of Ecology and Systematics 10:1-12.

Describes the interdependent relationship between figs and their pollinating wasps, focusing on the host-specificity of the wasps. Notes that alternate scenarios have been observed where: (a) More than one species of wasp is associated with a single species of fig (one species is a pollinator; secondary species apparently do not pollinate the plant). (b) One species of wasp is associated with more than one species of fig. Based on morphological phylogenies, the wasps and figs seem to match up at the level of wasp genera (or species groups) and sections of figs.

For a great look at this whole system, take a look at the Journal of Biogeography, July 1996, Volume 7, Issue 4. Whole issue focuses on both ecological and evolutionary aspects of fig trees and their associated animals.

Michaloud, G., Carriere, S. and Kobbi, M. 1996. Exceptions to the one:one relationship between African fig trees and their fig wasp pollinators: possible evolutionary scenarios. Journal of Biogeography 23: 513-520.

Amidst the 750 species-specific associations between figs and fig wasps are a few cases where this species-specificity breaks down (e.g.1 fig species having multiple wasp species). This paper presents some possible evolutionary scenarios that could explain the occurrence of these exceptions and makes some predictions about the future evolutionary outcome of these cases. These speciation scenarios are based on host shifts and subsequent habitat specialization.

Herre, E.A., Machado, C.A., Bermingham, E., Nason, J.D., Windsor, D.M., McCafferty, S.S., Van Houten, W., and Bachmann, K. 1996. Molecular phylogenies of figs and their pollinator wasps. Journal of Biogeography 23: 521-530.

Presents phylogenies for both the figs and wasps based on molecular data. This is probably the best attempt so far at using independent (molecular) data to examine the commonly accepted view that these obligate mutualists are an example of "strict sense coevolution". However, the phylogenies they produce do not have sufficient resolution to support or contradict the claims of "strict sense coevolution" that these authors make for this group.

Machado, C.A., Herre, E.A., McCafferty, S.S., and Bermingham, E. 1996. Molecular phylogenies of fig pollination and non-pollinating wasps and the implications for the origin and evolution of the fig-fig wasp mutualism. Journal of Biogeography 23: 531-542.

The wasp communities of figs often consist of three groups: pollinators (mutualists), non-pollinators (seed parasites), and parasitoids (which attack non-pollinating wasps). Uses molecular data to construct phylogenies in order to examine the degree of strict-sense coevolution between pollinating and non-pollinating wasps. Found high congruence between these two groups, suggesting the "predominance of strict-sense coevolution on shared host fig species". Found that pollinators form a monophyletic group. However, non-pollinating wasps do not. There is also a lot of potential for studying rates of evolution when comparing the phylogenies of the figs, pollinator and non-pollinator wasps, and their associated nematodes and mites.

Anstett, M.C., Hossaert-McKey, M., and Kjellberg, F. 1997. Figs and fig pollinators: evolutionary conflicts in a coevolved mutualism. Trends in Ecology and Evolution 12(3): 94-99.

This paper describes a lot of different ecological constraints that need to be met in order for coevolution to occur. It also discusses a range of ecological questions that could be addressed with phylogenetic data. This one can give you some familiarity with the details of the system in the context of coevolution.

The Yucca-Yucca moth system

Powell, Jerry A. 1992. Interrelationships of yuccas and yucca moths. Trends in Ecology and Evolution 7(1): 10-14.

Describes one of the textbook examples of coevolution and mutualism. While ovipositing into the flower's ovary, female yucca moths purposefully pollinate the plant. Reiterates that the correlation of associations between species of yucca moths and yuccas suggests the possibility of parallel cladogenesis between these groups. However, admits that further analysis awaits the production of phylogenies for the yuccas (Agavaceae). Covers many details of yucca and yucca moth biology, and summarizes many areas of study to date in this system.

Pellmyr, O., and Thompson, J.N. 1992. Multiple occurrences of mutualism in the yucca moth lineage. Proceedings of the National Academy of Sciences 89: 2927-2929.

Describes the biology of a close relative of the yucca moth. Draws parallels with the yucca moths in order to show that pollination mutualisms evolved more than once in this family (Lepidoptera: Prodoxidae). Calls for more studies regarding the evolution of (a) active pollination by ovipositing females and (b) loss of other copollinators for yuccas.

Pellmyr, Olle, and Huth, Chad J. 1994. Evolutionary stability of mutualism between yuccas and yucca moths. Nature 372: 257-260.

No phylogenies, but this ecological experiment is a very ingenious way to examine how the interaction between yuccas and yucca moths could be evolutionarily stable. Prevailing models suggest that stability only comes when both of the interacting species have ways of preventing excessive exploitation. These experiments suggest that yuccas can selectively abort flowers that bear heavy loads of yucca moth eggs. This means that moths laying many eggs are selected against, thereby maintaining the stability of the interaction.

Pellmyr, O., Thompson, J.N., Brown, J.M., and Harrison, R.G. 1996. Evolution of pollination and mutualism in the yucca moth lineage. The American Naturalist 148(5): 827-847.

Provides phylogenies based on combined molecular and morphological data for the moths. Experimentally test for the effectiveness of moth pollinators as it related to oviposition rates. Maps traits considered critical to the evolution of obligate mutualism onto the Prodoxid concensus tree: oviposition into flowers by females, limited seed destruction by larvae, and pollinator function. Present three hypotheses about the coevolution between yuccas and yucca moths: (1) Outline the reproductive traits for ancestral yuccas. (2) Describe the origins of and evolutionary path for the development of active pollination. (3) Describe why some yuccas have lost the ability to produce nectar. This is a very complete paper --- good to read IF you're really interested in the yucca-yucca moth system.

Pellmyr, O., and Leebens-Mack, J. 1999. Forty million years of mutualism: Evidence for Eocene origin of the yucca-yucca moth association. Proceedings of the National Academy of Science USA 96: 9178-9183.

Shows the extent to which phylogenetic methods have been used in plant-pollinator systems. Develops a molecular clock for the yucca moths and estimates the timing of major life history developments (colonization of woody monocots, colonization of yuccas, and becoming pollinators). Describes three alternative models for the development of this mutualism (strict cospeciation, synchronous diversification without cospeciation, and asynchronous diversification without cospeciation). However, good tests of yucca-yucca moth cospeciation await a strong yucca phylogeny.

SPECIALIZED MUTUALISMS: Other Examples

McDade, Lucinda A. 1992. Pollinator relationships, biogeography, and phylogenetics. Bioscience 42(1): 21-26.

This paper provides a phylogenetic analysis of a lineage of the genus Aphelandra (Acanthaceae) based on morphological traits. The pollination syndrome for each plant species is mapped on the tree to suggest that pollination by hermit hummingbirds (with long, decurved bills) is the ancestral trait, while pollination by trochiline hummingbirds (with shorter, strait bills) is a derived trait that evolved independently two times in this plant group. This author also examines biogeographic data for these species and concludes that obligate mutualistic relationships can act as a constraint on the evolution of the organisms (plant) that requires the mutualist's (pollinator) services.

Chase, Mark W. and Hills, Harold G. 1992. Orchid phylogeny, flower sexuality, and fragrance-seeking. Bioscience 42(1): 43-49.

Good description of the methods used in molecular and phylogenetic analysis. Present a tree for eight orchid subtribes based on molecular data. Map the various pollinator syndromes on the tree (pollination by male and female euglossine bees, pollination exclusively by male euglossine bees, or non-euglossine pollination) to suggest that pollination by male and female euglossines is the ancestral characteristic for the group. Interpret their results to support evolutionary scenarios based on previously acquired fossil data and artificial hybridization studies.

Widmer, A., Soliva, M., Erhardt, A., and Roy, B.A. 1998. Testing speciation mechanisms in orchids with molecular and ecological methods. Bulletin of the Geobotanical Institute ETH 64: 103-107.

Addresses the issue of whether mutualistic pollinators could drive floral speciation. They suggest that this pollinator-mediated directional selection on floral traits could occur as long as (a) "gene flow does not counter-balance selection", (b) there is little variation in pollinator abundance and efficiency, and (c) there is no opposing selection pressure coming from alternative pollinators or pathogens.

Armbruster, W. Scott. 1993. Evolution of plant pollination systems: Hypotheses and tests with the Neotropical vine Dalechampia. Evolution 47(5): 1480-1505.

Develops a phylogeny for 40 species of Dalechampia (Euphorbiaceae) based on morphological characters. Maps the pollination systems for each Dalechampia species onto a consensus tree, trying to determine the evolutionary development of different floral rewards (pollen, resin, or fragrance). Concludes that (a) pollination by male euglossine bees originated independently 3-4 times, (b) pollination by resin-collecting originated only once. In general, changes in pollination systems are evolutionarily labile in this genus.

Goldblatt, Peter and Manning, John C. 1996. Phylogeny and speciation in Lapeirousia subgenus Lapeirousia (Iridaceae: Ixioideae). Annals of the Missouri Botanical Gardens 83(3): 346-361.

Based on a morphological phylogeny of this plant group, these authors suggest that as plant floral morphology changed, the pollinator syndromes changed. For example, they suggested that as the length of the plant's perianth tube shortened over evolutionary time, the plants correspondingly shifted from pollination by long-tongued flies and sphinx moths to pollination by bees and smaller moths. They conclude that there is no evidence of pollinator-driven speciation in this plant group.

Fleming, Theodore H. and Holland, J. Nathaniel. 1998. The evolution of obligate pollination mutualisms: senita cactus and senita moth. Oecologia 114: 368-375.

This study experimentally assesses the interaction between the senita cactus and senita moth to determine if this is a new example of an obligate mutualism. Performed hand pollination and pollinator-exclusion experiments to determine that the interaction is mutualistic. Describes similarities between this and the yucca-yucca moth system (active pollination, nocturnal flower opening, self-incompatible breeding systems, resource-limited fruit production). Calls for phylogenetic studies to clarify the evolutionary relationship between senita cacti and senita moths.

Kress, W. John. 1993. Coevolution of plants and animals: Pollination of flowers by primates in Madagascar. Current Science 65(3): 253-257.

This paper makes weakly-supported claims about the development of pollination systems in the Strelitziaceae. The author suggests that pollination by lemurs is the archaic system, while pollination by birds and bats is the derived system. While his argument is logical, he doesn't really provide the "sufficient evidence" he claims to have. However, the question remains interesting, and this paper provides a somewhat unique investigation with mammalian pollinators.

Pellmyr, Olle. 1992. The phylogeny of a mutualism: evolution and coadaptation between Trollius and its seed-parasitic pollinators. Biological Journal of the Linnean Society 47: 337-365.

Does a good job of documenting the ecology of the interaction and geographical associations between the plants and the flies. Propose an admittedly uncertain phylogeny of the host plants (Trollius spp.) based on morphological characters.

Despres, L., and Jaeger, N. 1999. Evolution of oviposition strategies and speciation in the globeflower flies Chiastocheta spp. (Anthomyiidae). Journal of Evolutionary Biology 12: 822-831.

Makes it clear that this is another example of an obligate plant-pollinator mutualism. This system has several congeneric fly species living together on a single plant species (Triollius europaeus). Authors want to know how this system evolved and how it is maintained. Used a molecular phylogeny of the flies to suggest that mutualistic seed-feeding and pollination is the ancestral oviposition strategy, while seed parasitism without pollination is the derived strategy. They also suggest that the diversification in this fly community was not driven by cospeciation or host shifting, but more likely by sympatric reproductive isolation (via niche partitioning for oviposition sites). A very interesting system.