Ecological specialization in mycorrhizal symbiosis leads to rarity in an endangered orchid

Swarts, N; Sinclair, Elizabeth A.; Francis, Anthony; Dixon, Kingsley W.

doi:10.1111/j.1365-294x.2010.04736.x

Cited by 137 publications

(141 citation statements)

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“…By comparison, parasitisms having relatively high species-specificity have been shown to involve switching between more distantly related plants [42]. Generally, host-range limits vary between antagonistic associations compared to symbioses and mutualisms where narrower species-to-species dependencies are more common [43-45]. Parasites of the galling habit exhibit wider host ranges than that of the prey species and evolve host-plant conservatism as a secondary association [46,47].…”

Section: Discussionmentioning

confidence: 99%

Delayed colonisation of Acacia by thrips and the timing of host-conservatism and behavioural specialisation

2013

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BackgroundRepeated colonisation of novel host-plants is believed to be an essential component of the evolutionary success of phytophagous insects. The relative timing between the origin of an insect lineage and the plant clade they eat or reproduce on is important for understanding how host-range expansion can lead to resource specialisation and speciation. Path and stepping-stone sampling are used in a Bayesian approach to test divergence timing between the origin of Acacia and colonisation by thrips. The evolution of host-plant conservatism and ecological specialisation is discussed.ResultsResults indicated very strong support for a model describing the origin of the common ancestor of Acacia thrips subsequent to that of Acacia. A current estimate puts the origin of Acacia at approximately 6 million years before the common ancestor of Acacia thrips, and 15 million years before the origin of a gall-inducing clade. The evolution of host conservatism and resource specialisation resulted in a phylogenetically under-dispersed pattern of host-use by several thrips lineages.ConclusionsThrips colonised a diversity of Acacia species over a protracted period as Australia experienced aridification. Host conservatism evolved on phenotypically and environmentally suitable host lineages. Ecological specialisation resulted from habitat selection and selection on thrips behavior that promoted primary and secondary host associations. These findings suggest that delayed and repeated colonisation is characterised by cycles of oligo- or poly-phagy. This results in a cumulation of lineages that each evolve host conservatism on different and potentially transient host-related traits, and facilitates both ecological and resource specialisation.

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Section: Discussionmentioning

confidence: 99%

Delayed colonisation of Acacia by thrips and the timing of host-conservatism and behavioural specialisation

2013

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“…Mycorrhizal fungi can affect the diversity of plant communities (Van der Heijden et al. 1998) and potentially the distribution of plant species (Swarts et al. 2010).…”

Section: Introductionmentioning

confidence: 99%

“…While the rarity of species has been linked to a wide range of ecological traits (Schemske et al. 1994; Bevill & Louda 1999), only one previous study has tested the role of mycorrhizal fungi in causing rarity of the host (Swarts et al. 2010).…”

Section: Introductionmentioning

confidence: 99%

Do mycorrhizal symbioses cause rarity in orchids?

et al. 2011

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Summary 1. While rarely tested, the rarity of a species may be linked to the rarity of symbiotic partners. The requirement of many terrestrial plants to form a symbiosis with mycorrhizal fungi may limit the distribution and abundance of plant species. Here, in just the second test of the role of mycorrhiza in host species rarity, we investigate the influence of mycorrhizal specificity, distribution and ecological requirements in the genus Drakaea (Orchidaceae). 2. In situ seed baiting was used to resolve the distribution of mycorrhizal fungi for three common and two co‐occurring rare species of Drakaea. Mycorrhizal fungi were isolated from wild adult orchids and protocorms and the ITS nrDNA regions sequenced. An in vitro study tested the range of Drakaea species of which each fungus can support germination. 3. All Drakaea species studied used a narrow monophyletic clade of Tulasnella endophyte for protocorm, seedling and adult plant stages. In situ seed baiting revealed that germination of Drakaea is largely restricted to the same microhabitat as that of the orchid. However, within this habitat Drakaea exhibit comparable germination to other Western Australian orchid genera. Rare and common Drakaea exhibited no difference in germination rates and both germinated in suitable habitat not currently occupied. 4. Synthesis. In contrast to the previous study of the role of mycorrhiza in plant rarity, there was no evidence that mycorrhizal specificity contributed to rarity in Drakaea. However, the formation of mycorrhiza being mostly restricted to a specific microhabitat may limit the abundance of Drakaea in some landscapes. In Drakaea, the highly specific pollination system of sexual deception may contribute to rarity. A trend towards high specificity in orchid mycorrhizal associations in southern Australia is hypothesized to result from the predominance of old landscapes affording the opportunity for specialization on a single or few mycorrhiza(s) best adapted to the landscape conditions.

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“…Orchid species that associate with a limited number of fungi or fungi with a narrow distribution area can be hypothesized to be more vulnerable to changes in mycorrhizal abundances than orchid species that associate with a large suite of mycorrhizal fungi or fungi with a very broad distribution [10]–[12]. Although convincing evidence is still lacking, recent analyses of mycorrhizal associations in the Australian genus Caladenia have shown that mycorrhizal associations combined with other environmental factors can have a strong influence on plant rarity [12]. On the other hand, no relationship was found between orchid rarity and mycorrhizal specificity in the genus Drakaea .…”

Section: Introductionmentioning

confidence: 99%

Variation in Mycorrhizal Associations with Tulasnelloid Fungi among Populations of Five Dactylorhiza Species

et al. 2012

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BackgroundOrchid species rely on mycorrhizal symbioses with fungi to complete their life cycle. Although there is mounting evidence that orchids can associate with several fungi from different clades or families, less is known about the actual geographic distribution of these fungi and how they are distributed across different orchid species within a genus.Methodology/Principal FindingsWe investigated among-population variation in mycorrhizal associations in five species of the genus Dactylorhiza (D. fuchsii, D. incarnata, D. maculata, D. majalis and D. praetermissa) using culture-independent detection and identification techniques enabling simultaneous detection of multiple fungi in a single individual. Mycorrhizal specificity, determined as the number of fungal operational taxonomic units (OTUs), and phylogenetic diversity of fungi were compared between species, whereas discriminant analysis was used to compare mycorrhizal spectra across populations and species. Based on a 95% cut-off value in internal transcribed spacer (ITS) sequence similarity, a total of ten OTUs was identified belonging to three different clades within the Tulasnellaceae. Most OTUs were found in two or more Dactylorhiza species, and some of them were common and widespread, occurring in more than 50% of all sampled populations. Each orchid species associated with at least five different OTUs, whereas most individuals also associated with two or more fungal OTUs at the same time. Phylogenetic diversity, corrected for species richness, was not significantly different between species, confirming the generality of the observed orchid mycorrhizal associations.Conclusions/SignificanceWe found that the investigated species of the genus Dactylorhiza associated with a wide range of fungal OTUs from the Tulasnellaceae, some of which were widespread and common. These findings challenge the idea that orchid rarity is related to mycorrhizal specificity and fungal distribution.

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Ecological specialization in mycorrhizal symbiosis leads to rarity in an endangered orchid

Cited by 137 publications

References 51 publications

Delayed colonisation of Acacia by thrips and the timing of host-conservatism and behavioural specialisation

Delayed colonisation of Acacia by thrips and the timing of host-conservatism and behavioural specialisation

Do mycorrhizal symbioses cause rarity in orchids?

Variation in Mycorrhizal Associations with Tulasnelloid Fungi among Populations of Five Dactylorhiza Species

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