Vertical and horizontal photobiont transmission within populations of a lichen symbiosis

Abstract

Lichens are widespread symbioses and play important roles in many terrestrial ecosystems. The genetic structure of lichens is the result of the association between fungal and algal populations constituting the lichen thallus. Using eight fungus- and seven alga-specific highly variable microsatellite markers on within-population spatial genetic data from 62 replicate populations across Europe, North America, Asia and Africa, we investigated the contributions of vertical and horizontal transmission of the photobiont to the genetic structure of the epiphytic lichen Lobaria pulmonaria. Based on pairwise comparisons of multilocus genotypes defined separately for the mycobiont and for the photobiont, we inferred the transmission mode of the photobiont and the relative contribution of somatic mutation and recombination. After constraining the analysis of one symbiont to pairs of individuals with genetically identical symbiotic partners, we found that 77% of fungal and 70% of algal pairs were represented by clones. Thus, the predominant dispersal mode was by means of symbiotic vegetative propagules (vertical transmission), which dispersed fungal and algal clones co-dependently over a short distance, thus shaping the spatial genetic structure up to distances of 20m. Evidence for somatic mutation generating genetic diversity was found in both symbionts, accounting for 30% of pairwise comparisons in the alga and 15% in the fungus. While the alga did not show statistically significant evidence of recombination, recombination accounted for 7.7% of fungal pairs with identical algae. This implies that, even in a mostly vegetatively reproducing species, horizontal transmission plays a role in shaping the symbiotic association, as shown in many coral and other symbioses in nature.

Exploring symbiont management in lichens

“…It has been previously shown that dispersal of vegetative propagules is spatially limited in L. pulmonaria (Walser 2004), and the present work of Dal Grande et al (2012) shows that the signal for vertical transmission is cut in half over distances of 10 m. Vegetative propagules represent minute thallus initials that are larger, heavier and less aerodynamic than fungal spores. However, vertical transmission conveys clear advantages, including bypassing the bottleneck of biont resynthesis and, once established and producing sexual structures, opening the possibility for experimentation with new biont lineages under new microhabitat conditions.…”

“…These different dispersal strategies ostensibly shape the population genetic structure of lichen symbioses, but the relative contributions of vertical (joint) and horizontal (independent) symbiont transmission have long eluded lichen evolutionary biologists. In this issue of Molecular Ecology, Dal Grande et al (2012) close in on this question with the lung lichen, Lobaria pulmonaria, a flagship species in the conservation of old growth forests. By capitalizing on available microsatellite markers for both fungal and algal symbionts, they show that while vertical transmission is the predominant mode of reproduction, horizontal transmission is demonstrable and actively shapes population genetic structure.…”

“…Until now, it has been unclear to what extent sexual propagation horizontally reshapes the genetic structure of the component bionts of L. pulmonaria by reshuffling fungal and algal genotypes otherwise transmitted vertically in prepacked, joint vegetative propagules. In their study, Dal Grande et al (2012) use eight fungal and seven algal microsatellite markers to parse the contribution of horizontal and vertical transmission to the genetic structure of L. pulmonaria populations. By restricting the analysis for one symbiont to pairs of lichen thalli with genetically identical symbiotic partners, they show that 77% of fungal and 70% of algal pairs are represented by clones.…”

Reproduction, symbiosis, and the eukaryotic cell

“…Lichen, which are symbiotic associations between fungi and photosynthetic partners (algae and/or cyanobacteria), are another mixed case. Many lichen combine an asexual mode of reproduction in which propagules are made that contain samples of both partners, with sexual reproduction by the fungus through release of spores which, on germination, must find a compatible photosynthetic partner (29). A lichen then reproduces as a single unit when in asexual mode but not when the fungus reproduces sexually.…”

Genetic diversity of sterile culturedTrebouxiaphotobionts associated with the lichen-forming fungusXanthoria parietinavisualized with RAPD-PCR fingerprinting techniques

“…ITS phylogenies are based on only one locus, but genetic diversity at the subspecific level is best explored with a multilocus approach. Fingerprinting techniques can provide valuable data on the genetic diversity of populations and these have been successfully used for characterizing lichen-forming fungi at the subspecific level: microsatellite-based fingerprinting (Walser et al 2003;Walser et al 2005;Werth et al 2006;Werth et al 2007;Widmer et al 2010;Mansournia et al 2011;Dal Grande et al 2012), tRNA fingerprinting (Schmitt et al 2002), or randomly amplified polymorphic DNA (RAPD) analysis applied to either pure fungal material such as central strands of Usnea sp. (Heibel et al 1999) or apothecial discs (Printzen et al 1999), or to sterile cultured fungal isolates (Murtagh et al 1999;Dyer et al 2001;Honegger et al 2004b;Honegger & Zippler 2007;Itten & Honegger 2010).…”