Phylogenetic congruence of lichenised fungi and algae is affected by spatial scale and taxonomic diversity

Abstract

The role of species’ interactions in structuring biological communities remains unclear. Mutualistic symbioses, involving close positive interactions between two distinct organismal lineages, provide an excellent means to explore the roles of both evolutionary and ecological processes in determining how positive interactions affect community structure. In this study, we investigate patterns of co-diversification between fungi and algae for a range of New Zealand lichens at the community, genus, and species levels and explore explanations for possible patterns related to spatial scale and pattern, taxonomic diversity of the lichens considered, and the level sampling replication. We assembled six independent datasets to compare patterns in phylogenetic congruence with varied spatial extent of sampling, taxonomic diversity and level of specimen replication. For each dataset, we used the DNA sequences from the ITS regions of both the fungal and algal genomes from lichen specimens to produce genetic distance matrices. Phylogenetic congruence between fungi and algae was quantified using distance-based redundancy analysis and we used geographic distance matrices in Moran’s eigenvector mapping and variance partitioning to evaluate the effects of spatial variation on the quantification of phylogenetic congruence. Phylogenetic congruence was highly significant for all datasets and a large proportion of variance in both algal and fungal genetic distances was explained by partner genetic variation. Spatial variables, primarily at large and intermediate scales, were also important for explaining genetic diversity patterns in all datasets. Interestingly, spatial structuring was stronger for fungal than algal genetic variation. As the spatial extent of the samples increased, so too did the proportion of explained variation that was shared between the spatial variables and the partners’ genetic variation. Different lichen taxa showed some variation in their phylogenetic congruence and spatial genetic patterns and where greater sample replication was used, the amount of variation explained by partner genetic variation increased. Our results suggest that the phylogenetic congruence pattern, at least at small spatial scales, is likely due to reciprocal co-adaptation or co-dispersal. However, the detection of these patterns varies among different lichen taxa, across spatial scales and with different levels of sample replication. This work provides insight into the complexities faced in determining how evolutionary and ecological processes may interact to generate diversity in symbiotic association patterns at the population and community levels. Further, it highlights the critical importance of considering sample replication, taxonomic diversity and spatial scale in designing studies of co-diversification.

Comparison of phylogeographical structures of a lichen‐forming fungus and its green algal photobiont in western North America

“…In addition, the large spatial scale might result in limited availability of one or both partners relative to the other, which could also drive patterns in phylogenetic congruence (Buckley et al ., ). This pattern has been evidenced by examples from comparative phylogenetic studies in Ramalina (Buckley et al ., ) and in Caloplaca (Vargas Castillo & Beck, ). Spatial scales might also be important for explaining the co‐phylogeographical structure revealed in this study.…”

“…Similarly, we observed genetic structure among clades in both the mycobionts and the photobionts of the lichen R. menziesii, which is consistent with multiple ancient lineages in the mycobiont that could have evolved in separate refugia across western North America . In addition, the large spatial scale might result in limited availability of one or both partners relative to the other, which could also drive patterns in phylogenetic congruence (Buckley et al, 2014). This pattern has been evidenced by examples from comparative phylogenetic studies in Ramalina (Buckley et al, 2014) and in Caloplaca (Vargas Castillo & Beck, 2012).…”

“…It appears that the greatest likelihood for co‐evolution in lichen symbionts will occur when the two taxa are co‐dispersed (Büdel & Scheidegger, ; Bongaerts et al ., ). Nonetheless, some degree of co‐evolution might be possible for symbionts that are dispersed independently because they share niches and spatial distributions and many lichen fungi associate with only a small spectrum of algal clades and strains (Buckley et al ., ). Phylogeographical congruence may reflect co‐evolution or it may simply be due to common geographical or ecological barriers subjecting both symbionts to the parallel actions of genetic differentiation.…”

“…For example, two symbionts could show co-divergence when the population of one symbiont splits at the same time as that of its partner's population (Parker & Spoerke, 1998;Althoff & Thompson, 1999;Thompson & Cunningham, 2002;de Vienne et al, 2013). Unique local or regional environmental conditions can create selection pressures that favour parallel specialization and possible selection against non-local genotypes, thus leading to congruent genetic structure of both symbionts (Werth, 2010;Werth & Sork, 2010;del Campo et al, 2013;Rodelo-Urrego et al, 2013;Buckley et al, 2014). In addition, historical climatic oscillations, such as those during the Quaternary (Comes & Kadereit, 1998;Hewitt, 2004), could result in co-migration to new sites with suitable environmental conditions (Taberlet et al, 1998;Arbogast & Kenagy, 2001;Soltis et al, 2006).…”

Vulcanochloris (Trebouxiales, Trebouxiophyceae), a new genus of lichen photobiont from La Palma, Canary Islands, Spain

“…Although the biogeography of microorganisms has become a highly discussed topic (Caron 2009), investigations dealing with the biogeography of symbiotic protists are still very scarce. The population studies on lichenized Trebouxia species indicated that the distribution of particular genotypes is particularly shaped by either climatic factors (Fernández-Mendoza et al 2011) or distribution patterns of mycobiont partners (Buckley et al 2014). The single study dealing with the biogeography of Asterochloris photobionts indicated generally cosmopolitan distribution of species (Řídká et al 2014).…”