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Bernard Slippers1, 2, Rimvis Vasiliauskas2, Brett Hurley1, Jan Stenlid2 and Michael J Wingfield1
1 Tree Protection Co-operative Programme, Forestry and Agricultural
Biotechnology Institute, University of Pretoria, Pretoria, South Africa
2 Department of Forest Mycology and Pathology, Swedish University of Agricultural Biotechnology Institute, Uppsala, Sweden
The Forestry and Agricultural Biotechnology Institute, University of
Pretoria and the Department of Forest Mycology and Pathology, Swedish
University of Agricultural Biotechnology Institute, Uppsala, Sweden are
collaborating on a study of the Siricid-Fungal symbiosis, and its
parasites. This project aims to address questions in two general areas,
namely (a) the evolution and biology of mutualistic symbiosis and (b)
the monitoring and control of wood inhabiting pests and pathogens that
threaten biodiversity and forest production in introduced and native
environments.
Project background
The symbiosis between woodwasps and fungi (Fig. 1)
Figure 1. Life-cycle of Siricid woodwasps and their Amylostereum symbiotic fungi.
A mutualistic symbiosis exists between Siricid woodwasps and
Amylostereum fungi [1, 2]. The relationship between these organisms is
specialised and obligatory species specific, at least for the insects.
The principle advantage for the fungus is that it is spread and
inoculated into suitable wood substrates during wasp oviposition. In
turn, the fungus rots and dries the wood, providing a suitable
environment, nutrients and enzymes to the developing insect larvae.
The burrowing activity of the Siricid larvae and fungal white rot of
the wood make this insect-fungus symbiosis potentially harmful to its
conifer host trees. However, in the northern hemisphere, where the
Siricidae are native, the insect is of little economic importance,
except during times of increased stress due to other factors [3]. Here
a natural balance exists between the insect-fungus complex, its natural
parasites and host trees as long as the trees are generally healthy.
These organisms have been studied widely in Europe to understand their
fascinating biology.
Amylostereum spp. are Basidiomycetes that are heterothallic and have a
tetrapolar nuclear state [4]. Such a mating system increases
outcrossing and thus normally also population diversity. The
Amylostereum spp. are, however, also spread by woodwasps in the form of
asexually produced oidia (thus genetically identical) [5].
In the northern hemisphere clonal lines of A. areolatum and A.
chailletii are preserved over time and occur over large areas as a
result of the spread of oidia of by woodwasps [5-7]. This situation is
even more dramatic in the southern hemisphere where a single vegetative
compatibility group (VCG) dominates populations of A. areolatum
associated with S. noctilio [8]. Isolates from South Africa, Brazil and
Uruguay represent the same VCG. This VCG in turn was partially
compatible with isolates from New Zealand and Tasmania. These results
suggest that the spread of Sirex through the southern hemisphere during
this century has taken place among the continents and countries of this
region, rather than by separate introductions from the northern
hemisphere. The results, further, indicate that A. areolatum in the
southern hemisphere spreads exclusively asexually through its
association with S. noctilio. No sporocarps of A. areolatum have thus
far been found in the southern hemisphere.
Woodwasp-fungal symbionts as forest pests and their control
There is an increasing number of exotic pest and pathogen invasions
that threaten the world’s ecosystems [9, 10]. Many of these
introductions have had or are having catastrophic outcomes. The
long-term sustainability of native forest and forestry industries will
depend on the capacity to effectively deal with such introduced insect
pests and pathogens.
Forests in Europe are increasingly at risk from newly introduced
pathogens, continued human pressure and alteration of habitat, as well
as global weather changes. Evidence of this has been numerous
emergences of disease outbreaks or species ‘declines’ across Europe.
Dutch-elm disease and Oak decline in central and southern Europe,
Fraxinus decline in northern Europe, Pinus dieback in various areas in
Europe, Ostrya decline in southern Europe, etc. The current amount of
freshly dead wood (75 mil m3) in Sweden following the storm of January
2005 adds to this risk for native forests as many Siricids prefer such
material to bread in [3]. Significant increases in Siricid populations,
coupled with the pressures mentioned above, can hold significant risks
for attacks on stored (unharvested) timber and standing trees weakened
by other pests (e.g. bark beetles and Armillaria root rot). Such a
situation exists in parts of Switzerland (Dr. U. Heiniger, pers.
comm.).
Sirex noctilio and A. areolatum have been introduced into various
southern hemisphere countries and, recently, to the USA (where it is
currently viewed as a potential threat to forest health) [11, 12]. In
contrast to the native range, these symbiotic organisms have caused
extensive mortality in exotic pine plantations in the southern
hemisphere [13, 14]. Despite the costly efforts to monitor and control
the wasp and fungus during the previous century, the pest complex
continues to kill significant numbers of trees and spread to previously
unaffected areas in Australia, South Africa and South America. In many
of these regions this pest complex is considered to be the biggest
threat to pine forestry operations.
Sirex noctilio is most effective controlled through biological control
agents such as the nematode Deladenus siricidicola and some parasitic
wasp species, in combination with silvicultural practices aimed at
reducing tree stress [15, 16]. The nematode is, however, the main form
of control. Deladenus siricidicola has a closely co-evolved and
integrated life cycle with both the wasp and fungal symbiont (Fig. 2).
For this reason, the efficiency of biocontrol programmes is often
affected by the specific nematode strain or fungal strain involved.
Wasp parasites are currently underused in many countries due to
incomplete information from native ranges and weak application
strategies.
Figure 2. Bicyclic life cycle of the Sirex biocontrol nematode,
Deladenus siricidicola. (Adapted from Bedding 1972, Nematologica)
General questions addressed in the project
Molecular techniques have only recently been applied to questions
pertaining to Amylostereum taxonomy, phylogeny and population
structures [17-20]. These studies have clarified previous hypotheses
that were based on morphological and mating studies, regarding the
relationships among Amylostereum spp. They have also raised new and
challenging questions regarding the identity of the fungal isolates
associated with certain woodwasps. From these preliminary observations
there appear to be cryptic speciation that have been overlooked using
traditional methods of identification. On a higher taxonomic level, the
relationship of Amylostereum to other Basidiomycetes is currently
unsure due to contradictory literature reports [11].
A study of the population structure of Amylostereum fungi from many
parts of the world, using both VCG’s and molecular markers, will give
valuable insight into the geographical origin and spread of these
fungi, as well as their associated Siricid wasps. Such data have
already identified patterns of spread amongst countries in the southern
hemisphere and between some local populations in Scandinavia [5-7, 20].
Phylogeographic data is, however, lacking for most of natural
distribution of Siricids and their fungi. The northern hemisphere
origins of southern hemisphere populations of Sirex and Amylostereum
are not known, despite its importance for selection of control agents.
Despite detailed studies of the symbioses between Siricid woodwasps and
their fungal symbionts, many fundamental questions remain unanswered.
For example, it is thought that vertical transmission (from mother to
daughter) predominates. However, the numerous wasp species apparently
carrying the same fungal species indicate some level of horizontal
transfer of the symbiont between wasp species. The importance of such
data is illustrated by the lack of any explanation of the fundamental
differences in population structures of A. areolatum (highly clonal)
and A. chailetii (almost indistinguishable from population structures
of other basidiomycetes spreading through sexual spores). Furthermore,
there is no co-evolutionary or phylogeographic data on which to infer
the evolutionary development of the symbiosis. The lack of this
information also excludes the comparison of this symbiosis with other
symbiotic systems.
Siricid-like wasps are known from the Jurassic period (more than 150
mya) [21]. Parallels between the Siricid-fungal symbiosis and other
independently derived symbioses are likely to reveal evolutionary
factors that are important for the development and stability of such
partnerships. Such a co-evolved system also presents important
opportunities to study comparative rates of molecular evolution in
different symbiotic partners, and non-symbiotic relatives, as well as
addressing general questions of the adaptive significance of sex [22].
The artificial selection during mass rearing of biological control
agents in control programmes can lead to severe bottlenecks in
populations of these organisms. This will severely reduce population
diversity in the control organisms, which will reduce their ability to
respond to changes in the environment or host. During the nematode
rearing process the accidental selection of less infective strains of
D. siricidicola has lead to a temporary breakdown of the biological
control programme in Australia, resulting in huge damages [16]. Despite
these dangers, there is currently no data or methods available to study
populations, compare strains or track changes in populations of the
biological control organisms.
In order to conduct this study, collections of populations of wasps,
fungi and biocontrol agents are needed to represent the native
occurrence of these organisms, as well as areas where they have been
introduced. Collected samples from the southern hemisphere (Argentina,
Brazil, Australia, South Africa) and Europe (Austria, Denmark, Great
Britain, Italy, Greece, Norway, Sweden, Switzerland) have been made in
collaboration with various other researchers and research organization.
This material is supplemented from international culture collections
and herbaria (Canada, France, Germany, Japan, Russia, USA). As part of
collecting efforts, potential attractants and methods have been
identified to catch woodwasps. These collections are ongoing.
Conclusion
It is hoped that the project will help unravel the evolutionary causes
and consequences of woodwasp-fungal symbiosis. Such basic information
will contribute to understanding fungal-insect symbiosis, as well as
symbiosis as a general biological theme influencing evolution of
organisms. In addition, such data will provide practical assistance to
monitoring and controlling programs of introduced population of Siricid
woodwasps and their symbiotic fungi. It will also help to characterize
patterns of natural and human-mediated spread of these insects. From
these data, the project should also contribute to the growing body of
knowledge concerning international movement and control of pests and
pathogens, to help prevent recurrence of such events.
Acknowledgements
We wish to thank the Tree Protection Co-operative Programme, Forestry
SA, University of Pretoria, Swedish University of Agricultural
Sciences, the SIDA-NRF South African – Swedish Research Partnership
Programme, NRF Postdoctoral Programme and the Skye Foundation for
financial support for this project.
References
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