EVOLUTIONARY ASSEMBLY OF TRITROPHIC INTERACTIONS: HOLARCTIC PLANTS, NEMATINE SAWFLIES, AND PARASITOIDS AS A TEST CASE

Female of Fallocampus americanus.

 

Male of Euura lanatae on Salix lanata.

 

Female of Pristiphora mollis ovipositing on Vaccinium myrtillus.

 

Larva of Nematus ribesii on Ribes uva-crispa.

 

Larva of the "palisade sawfly" Stauronematus compressicornis on Populus tremula.

 

Larva of Nematus miliaris on Salix aurita.

 

Pristiphora erichsonii larvae on Larix sp.

 

Trichiocampus viminalis larvae on Salix pyrolifolia.

 

Larva of Pristiphora sp. on Picea abies.

 

A flat, cryptic larva of Platycampus luridiventris resting next to the midrib of an Alnus incana leaf.

 

Larva of Melastola sp. in berry of Vaccinium parvifolium.

 

Larva of Pseudodineura enslini in leaf mine on Trollius altissimus.

 

Larva of a Pontopristia sp. catkin miner on Salix lapponum.

 

Galls of Pontania proxima on Salix fragilis.

 

Larva of Euura lapponica inside shoot gall on Salix lapponum.

Tommi Nyman


Department of Biology, University of Eastern Finland

P.O. Box 111, FI-80101 Joensuu, Finland

 

Phone: +358 40 520 6540

E-mail: Tommi.Nyman [at] uef.fi

 

 

How to assemble a multitrophic food web?

Most herbivorous insect species feed on only one or a few plant species, but it is known that the host-plant associations of any given insect lineage may change during evolutionary time scales. One of the “big questions” in evolutionary biology is what determines the speed and direction of these host shifts.

There is a growing consensus that the probability of shifts among plant taxa is affected by multiple factors, including host-plant chemistry, morphology, phenology, and ecology. Recently, the role of natural enemies has received increased attention, because enemy pressure could facilitate both ecological specialization and divergence in herbivorous insect lineages. Especially parasitoids cause severe mortality in natural insect populations, and if parasitoids use plants as ques for finding their prey, host shifts by herbivorous insects could be driven by "enemy-free space" provided by the novel host-plant species. Enemy-free space could, however, also be found by feeding internally on plant tissues, and it has also been suggested that parasitoid pressure has contributed to the enormous morphological diversity of galls that are induced by various insect groups on plants.

Plants, herbivorous insects, and their enemies form complex multitrophic food webs, but the evolutionary assembly of such interaction networks remains mostly unknown. Phylogenetic studies have begun to shed light on the complexities in insect-plant interactions, and earlier "strict" coevolutionary hypotheses have given way to more dynamic views: plant taxa are continuously being colonized from different insect lineages, so the insect community on any given plant lineage is a collection of species with widely varying degrees of coevolutionary history with the host. At the same time, a similar process goes on between the herbivores and their enemies, but the assembly of these interactions has thus far received far less attention.

We use the sawflies that belong to the subfamily Nematinae (Hymenoptera: Tenthredinidae) as a model group for studying the ongoing coevolution between plants, herbivorous insects, and parasitoids in the Holarctic region. The aim is to utilize phylogenetic methods to understand the evolutionary history of Nematinae, their host-plant associations, and their diverse natural enemies.

 

The study group

Nematinae is a taxonomically and ecologically diverse sawfly group that is distributed across the whole Northern Hemisphere. This monophyletic subfamily includes over 1000 species that can be divided into ca. 40 genera in eight tribes. Nematines constitute an ecologically prominent insect group especially in arctic and subarctic habitats. The larvae of most nematines feed on deciduous trees or shrubs, but conifers, herbs, and grasses are utilized by some species. Some of the most abundant nematines are serious pests of orchard and forest trees. Individual species are typically oligophagous on hosts belonging to one or a few related host genera, but the degree of specialization varies from strict monophagy on single host species to extreme polyphagy on over ten genera. The larval habits of nematines are equally diverse. While a majority of the species have larvae that feed externally on leaves or needles, the larvae of others live inside plant tissues. These endophagous groups mine inside leaves, petioles, buds, inflorescences, fruits, berries, or catkins. In addition, the larvae of some nematine groups live inside galls or leaf rolls induced by the ovipositing females.

The subfamily Nematinae provides a near-ideal model group for studying the evolutionary assembly of tritrophic food webs. Because nematines are common in northern areas, their host-plant associations are well documented. In addition, an extensive literature on their parasitoid complexes is available, and well over 150 parasitoid species representing many hymenopteran and dipteran families are known to attack various nematine species. As a result of our earlier and ongoing studies, the phylogeny and ecological history of Nematinae is fairly well known; our aim is now to combine the existing phylogenetic information with the data on host-plant use and parasitoid communities. Especially the gall-inducing nematines in the species-rich subtribe Euurina constitute a promising target for phylogenetic studies employing a multitrophic approach. [More on the subtribe Euurina: click here]

 

Main study questions

Our studies focus mainly on proposed "bottom-up" and "top-down" diversification effects that could span several trophic levels:

* Does colonization of species-rich plant groups such as Salix lead to elevated speciation rates in insects?

* How do switches among host plants and feeding niches affect the parasitoid assemblages of insect hebivores?

* Does release from parasitism increase speciation rates?

* Does speciation and/or ecological divergence on one trophic level affect diversification on the trophic levels above it, i.e., do "multitrophic speciation cascades" exist?

 

Published articles

Valtonen, M., Palo, J. U., Aspi, J., Ruokonen, M., Kunnasranta, M. & Nyman, T. 2014. Causes and consequences of fine-scale population structure in a critically endangered freshwater seal. BMC Ecology 14: e22. [Pdf]

Malm, T. & Nyman, T. 2014. Phylogeny of the symphytan grade of Hymenoptera: new pieces into the old jigsaw(fly) puzzle. Cladistics, in press. [Abstract]

Prous, M., Blank, S. M., Goulet, H., Heibo, E., Liston, A., Malm, T., Nyman, T., Schmidt, S., Smith, D. R., Vårdal, H., Viitasaari, M., Vikberg, V. & Taeger, A. 2014. The genera of Nematinae (Hymenoptera, Tenthredinidae). Journal of Hymenoptera Research, in press.

Boevé, J.-L., Blank, S. M., Meijer, G. & Nyman, T. 2013. Invertebrate and avian predators as drivers of chemical defensive strategies in tenthredinid sawflies. BMC Evolutionary Biology 13: e198. [Pdf]

Heimonen, K., Lwanga, J. S., Mutanen, M., Nyman, T. & Roininen, H. 2013. Spatial and temporal variation in community composition of herbivorous insects on Neoboutonia macrocalyx in a primary tropical rain forest. Journal of Tropical Ecology 29: 229–241. [Abstract]

Leppänen, S. A., Altenhofer, E., Liston, A. D. & Nyman, T. 2013. Ecological versus phylogenetic determinants of trophic associations in a plantleafminerparasitoid food web. Evolution 67: 14931502. [Abstract]

Caron, V., Norgate, M., Ede, F. J., Nyman, T. & Sunnucks, P. 2013. Novel microsatellite DNA markers indicate strict parthenogenesis and few genotypes in the invasive willow sawfly Nematus oligospilus. Bulletin of Entomological Research 103: 7481. [Abstract]

Valtonen, M., Palo, J. U., Ruokonen, M., Kunnasranta, M. & Nyman, T. 2012. Spatial and temporal variation in genetic diversity of an endangered freshwater seal. Conservation Genetics 13: 12311245. [Abstract]

Nyman, T., Linder, H. P., Peña, C., Malm, T. & Wahlberg, N. 2012. Climate-driven diversity dynamics in plants and plant-feeding insects. Ecology Letters 15: 889898. [Abstract]

Leppänen, S. A., Altenhofer, E., Liston, A. D. & Nyman, T. 2012. Phylogenetics and evolution of host-plant use in leaf-mining sawflies (Hymenoptera: Tenthredinidae: Heterarthrinae). Molecular Phylogenetics and Evolution 64: 331341. [Abstract]

Kaila, L., Mutanen, M. & Nyman, T. 2011. Phylogeny of the mega-diverse Gelechioidea (Lepidoptera): adaptations and determinants of success. Molecular Phylogenetics and Evolution 63: 801809. [Abstract]

Nyman, T., Paajanen, R., Heiska, S. & Julkunen-Tiitto, R. 2011. Preference–performance relationship in the gall midge Rabdophaga rosaria: insights from a common-garden experiment with nine willow clones. Ecological Entomology 36: 200211. [Abstract]

Nyman, T., Vikberg, V., Smith, D. R. & Boevé, J.-L. 2010. How common is ecological speciation in plant-feeding insects? A 'Higher' Nematinae perspective. BMC Evolutionary Biology 10: e266. [Pdf] [See related interview on Nature News 2.3.2011] [Article received BioMed Central's Open Data Award 6.5.2011]

Nyman, T. 2010. To speciate, or not to speciate? Resource heterogeneity, the subjectivity of similarity, and the macroevolutionary consequences of niche-width shifts in plant-feeding insects. Biological Reviews 85: 393411. [Pdf]

Liston, A. D., Nyman, T. & Kehl, A. 2007. The first report of gall induction in the sawfly subfamily Allantinae (Hymenoptera: Tenthredinidae). Entomologica Fennica 18: 199205. [Pdf] [Fig. 1 in colour]

Nyman, T., Bokma, F. & Kopelke, J.-P. 2007. Reciprocal diversification in a complex plantherbivoreparasitoid food web. BMC Biology 5: e49. [Pdf] [Featured on the EU's European Research Headlines on 16.11.2007]

Nyman, T., Farrell, B. D., Zinovjev, A. G. & Vikberg, V. 2006. Larval habits, host-plant associations, and speciation in nematine sawflies (Hymenoptera: Tenthredinidae). Evolution 60: 16221637. [Pdf] [Electronic Appendix] [Fig. 2 in colour]

Nyman, T., Zinovjev, A. G., Vikberg, V. & Farrell, B. D. 2006. Molecular phylogeny of the sawfly subfamily Nematinae (Hymenoptera: Tenthredinidae). Systematic Entomology 31: 569583. [Pdf] [Electronic Appendix]

Roller, L., Beneš, K., Blank, S. M., Holuša, J., Jansen, E., Jänicke, M., Kaluza, S., Kehl, A., Kehr, I., Kraus, M., Liston, A. D., Nyman, T., Nie, H., Savina, H., Taeger, A. & Wei, M. 2006. Contribution to the knowledge of sawfly fauna (Hymenoptera, Symphyta) of the Low Tatras National park in Central Slovakia. Naturae Tutela 10: 5772. [Pdf]

Nyman, T. & Julkunen-Tiitto, R. 2005. Chemical variation within and among six northern willow species. Phytochemistry 66: 28362843. [Pdf]

Roininen, H., Nyman, T. & Zinovjev, A. G. 2005. Biology, ecology, and evolution of gall-inducing sawflies (Hymenoptera: Tenthredinidae and Xyelidae). Pp. 467494 in Raman, A., Schaefer, C. W., and Withers, T. M., eds. Biology, Ecology, and Evolution of Gall-inducing Arthropods. Science Publishers, Inc., Enfield, NH.

Nyman, T., Ylioja, T. & Roininen, H. 2002. Host-associated allozyme variation in tree cambium miners, Phytobia spp. (Diptera: Agromyzidae). Heredity 89: 394400. [Pdf]

Nyman, T. 2002. The willow bud galler Euura mucronata Hartig (Hymenoptera: Tenthredinidae): one polyphage or many monophages? Heredity 88: 288295. [Pdf]

Nyman, T., Widmer, A. & Roininen, H. 2000. Evolution of gall morphology and host-plant relationships in willow-feeding sawflies (Hymenoptera: Tenthredinidae). Evolution 54: 526533. [Pdf] [Fig. 2 in colour]

Nyman, T. & Julkunen-Tiitto, R. 2000. Manipulation of the phenolic chemistry of willows by gall-inducing sawflies. Proc. Natl. Acad. Sci. USA 97: 1318413187. [Pdf] [Electronic Appendix]

Nyman, T., Roininen, H. & Vuorinen, J. A. 1998. Evolution of different gall types in willow-feeding sawflies (Hymenoptera: Tenthredinidae). Evolution 52: 465474. [Pdf]

 

PhD thesis

Nyman, T. 2000. Phylogeny and ecological evolution of gall-inducing sawflies (Hymenoptera: Tenthredinidae). University of Joensuu, PhD Dissertations in Biology 6: 192. [Pdf of summary part]

 

PhD students

Sanna Leppänen (Ecology and evolution of tritrophic interactions in leaf-mining and gall-inducing sawflies)

Mia Valtonen (Genetic diversity and population structure of the endangered Lake Saimaa ringed seal)

 

Insects on northern plants

*Gall inducers in the subtribe Euurina

*Leaf-mining sawflies in Tenthredinidae

*Insects on willows

*Insects on aspen

*Insects on birch

 

Request for sawfly samples

*Collection instructions

*Wish-list 2009

 

 

[Alternative CV]