Species in section Peltidea (aphthosa group) of the genus Peltigera remain cryptic after molecular phylogenetic revision

Magain, Nicolas; Hoz, Carlos J. Pardo‐De la; Niu, Dongling; Goward, Trevor; Sérusiaux, Emmanuël; Lutzoni, François

doi:10.2478/pfs-2018-0007

Cited by 15 publications

(27 citation statements)

References 67 publications

(110 reference statements)

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“… O’Brien et al (2013) found five different Nostoc phylogroups (I, III, IV, V, and VI) in association with species of the three trimembered sections of Peltigera , each species showing a different degree of specificity toward Nostoc phylogroups. An unusually high level of reciprocal specificity between Nostoc and P. malacea was detected by O’Brien et al (2013) , which was confirmed by Miadlikowska et al (2018) based on more specimens and additional loci. Based on a multi-locus phylogenetic study, Miadlikowska et al (2018) also found that several mycobiont clades within section Peltidea could potentially represent new species.…”

Section: Introductionmentioning

confidence: 55%

Contrasting Symbiotic Patterns in Two Closely Related Lineages of Trimembered Lichens of the Genus Peltigera

et al. 2018

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Species circumscription is key to the characterization of patterns of specificity in symbiotic systems at a macroevolutionary scale. Here, a worldwide phylogenetic framework was used to assess the biodiversity and symbiotic patterns of association among partners in trimembered lichens from the genus Peltigera, section Chloropeltigera. We sequenced six loci of the main fungal partner and performed species discovery and validation analyses to establish putative species boundaries. Single locus phylogenies were used to establish the identity of both photobionts, Nostoc (cyanobacterium) and Coccomyxa (green alga). Distribution and specificity patterns were compared to the closely related clade, section Peltidea, which includes mainly Peltigera species with trimembered thalli. For section Chloropeltigera, eight fungal species (including five newly delimited putative species) were found in association with nine Nostoc phylogroups and two Coccomyxa species. In contrast, eight fungal species (including three newly delimited putative species) in section Peltidea were found in association with only four Nostoc phylogroups and the same two Coccomyxa species as for section Chloropeltigera. This difference in cyanobiont biodiversity between these two sections can potentially be explained by a significantly higher frequency of sexual reproductive structures in species from section Chloropeltigera compared to section Peltidea. Therefore, horizontal transmission of the cyanobiont might be more prevalent in Chloropeltigera species, while vertical transmission might be more common in Peltidea species. All Peltigera species in section Chloropeltigera are generalists in their association with Nostoc compared to more specialized Peltigera species in section Peltidea. Constrained distributions of Peltigera species that associate strictly with one species of green algae (Coccomyxa subellipsoidea) indicate that the availability of the green alga and the specificity of the interaction might be important factors limiting geographic ranges of trimembered Peltigera, in addition to constraints imposed by their interaction with Nostoc partners and by climatic factors.

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Section: Introductionmentioning

confidence: 55%

Contrasting Symbiotic Patterns in Two Closely Related Lineages of Trimembered Lichens of the Genus Peltigera

et al. 2018

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“…We assembled a dataset of Peltigera-Nostoc interaction pairs summing up all information from the literature for which we could confidently assess the identity of the Peltigera species and Nostoc phylogroups or haplotypes (Chagnon et al, 2018;Lu et al, 2018;Magain, Miadlikowska, Goffinet, et al, 2017a;Magain, Miadlikowska, Mueller, et al, 2017b;Magain et al, 2018;Miadlikowska et al, 2014Miadlikowska et al, , 2018O'Brien, Miadlikowska, & Lutzoni, 2005;O'Brien, Miadlikowska, & Lutzoni, 2013;Pardo De la Hoz et al, 2018). The total dataset consisted of 1,026 thalli, or interaction pairs, representing 155 Peltigera species and 95 Nostoc phylogroups or haplotypes (Tables S1 and S2).…”

Section: Sample Acquisition and Interaction Network Inferencementioning

confidence: 99%

“…To infer a phylogeny for the entire genus Peltigera, we gathered published data from all currently validated species (Chagnon et al, 2018;Magain, Miadlikowska, Goffinet, et al, 2017a;Magain, Miadlikowska, Mueller, et al, 2017b;Magain et al, 2018;Miadlikowska et al, 2014Miadlikowska et al, , 2018Pardo De la Hoz et al, 2018) for seven loci (ITS, nrLSU, β-tubulin, RPB1, COR1b, COR3, COR16). We selected one representative per species with the highest number of sequenced loci, or two representatives per species when sets of available loci were mostly non-overlapping between two specimens of a species.…”

Section: Phylogeny Of the Genus Peltigeramentioning

confidence: 99%

“…Because each locus was analysed separately in previous studies to detect potential topological conflicts, with appropriate corrections made when needed (Chagnon et al, 2018;Magain, Miadlikowska, Goffinet, et al, 2017a;Magain, Miadlikowska, Mueller, et al, 2017b;Magain et al, 2018;Miadlikowska et al, 2014Miadlikowska et al, , 2018Pardo De la Hoz et al, 2018), we concatenated these seven loci using in-house PERL scripts (Magain, 2018). Our concatenated dataset consisted of 205 specimens and 10,064 characters.…”

Section: Phylogeny Of the Genus Peltigeramentioning

confidence: 99%

“…These modules include 1-to-1 strict F I G U R E 2 Close-ups of the seven-locus chronogram of the genus Peltigera: (a) POLY clade, that is, sections Chloropeltigera, Peltidea, Phlebia and Polydactylon, and (b) PELT clade, that is, sections Horizontales, Peltigera and Retifoveatae. Branch lengths are proportional to relative time, and each terminal tip represents a species indicated on the far right, or putative species resulting from recent studies (Magain, Miadlikowska, Goffinet, et al, 2017a;Magain et al, 2018;Pardo De La Hoz et al, 2018;Miadlikowska et al, 2018). The coloured capital letters immediately to the right of the terminal branch tips represent the network modules of each species, based on results of the modularity analyses (Figure 1).…”

Section: Eight Modules Consist Of Only One Peltigera Species and Onementioning

confidence: 99%

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Species diversification and phylogenetically constrained symbiont switching generated high modularity in the lichen genus Peltigera

2019

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Ecological interactions range from purely specialized to extremely generalized in nature. Recent research has showed very high levels of specialization in the cyanolichens involving Peltigera (mycobionts) and their Nostoc photosynthetic partners (cyanobionts). Yet, little is known about the mechanisms contributing to the establishment and maintenance of such high specialization levels. Here, we characterized interactions between Peltigera and Nostoc partners at a global scale, using more than one thousand thalli. We used tools from network theory, community phylogenetics and biogeographical history reconstruction to evaluate how these symbiotic interactions may have evolved. After splitting the interaction matrix into modules of preferentially interacting partners, we evaluated how module membership might have evolved along the mycobionts’ phylogeny. We also teased apart the contributions of geographical overlap vs phylogeny in driving interaction establishment between Peltigera and Nostoc taxa. Module affiliation rarely evolves through the splitting of large ancestral modules. Instead, new modules appear to emerge independently, which is often associated with a fungal speciation event. We also found strong phylogenetic signal in these interactions, which suggests that partner switching is constrained by conserved traits. Therefore, it seems that a high rate of fungal diversification following a switch to a new cyanobiont can lead to the formation of large modules, with cyanobionts associating with multiple closely retated Peltigera species. Finally, when restricting our analyses to Peltigera sister species, the latter differed more through partner acquisition/loss than replacement (i.e., switching). This pattern vanishes as we look at sister species that have diverged longer ago. This suggests that fungal speciation may be accompanied by a stepwise process of (a) novel partner acquisition and (b) loss of the ancestral partner. This could explain the maintenance of high specialization levels in this symbiotic system where the transmission of the cyanobiont to the next generation is assumed to be predominantly horizontal. Synthesis. Overall, our study suggests that oscillation between generalization and ancestral partner loss may maintain high specialization within the lichen genus Peltigera, and that partner selection is not only driven by partners’ geographical overlap, but also by their phylogenetically conserved traits.

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Phylogenetic structure of specialization: A new approach that integrates partner availability and phylogenetic diversity to quantify biotic specialization in ecological networks

Hoz

Medeiros

Gibert

et al. 2022

Ecology and Evolution

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Biotic specialization holds information about the assembly, evolution, and stability of biological communities. Partner availabilities can play an important role in enabling species interactions, where uneven partner availabilities can bias estimates of biotic specialization when using phylogenetic diversity indices. It is therefore important to account for partner availability when characterizing biotic specialization using phylogenies. We developed an index, phylogenetic structure of specialization (PSS), that avoids bias from uneven partner availabilities by uncoupling the null models for interaction frequency and phylogenetic distance. We incorporate the deviation between observed and random interaction frequencies as weights into the calculation of partner phylogenetic α‐diversity. To calculate the PSS index, we then compare observed partner phylogenetic α‐diversity to a null distribution generated by randomizing phylogenetic distances among the same number of partners. PSS quantifies the phylogenetic structure (i.e., clustered, overdispersed, or random) of the partners of a focal species. We show with simulations that the PSS index is not correlated with network properties, which allows comparisons across multiple systems. We also implemented PSS on empirical networks of host–parasite, avian seed‐dispersal, lichenized fungi–cyanobacteria, and hummingbird pollination interactions. Across these systems, a large proportion of taxa interact with phylogenetically random partners according to PSS, sometimes to a larger extent than detected with an existing method that does not account for partner availability. We also found that many taxa interact with phylogenetically clustered partners, while taxa with overdispersed partners were rare. We argue that species with phylogenetically overdispersed partners have often been misinterpreted as generalists when they should be considered specialists. Our results highlight the important role of randomness in shaping interaction networks, even in highly intimate symbioses, and provide a much‐needed quantitative framework to assess the role that evolutionary history and symbiotic specialization play in shaping patterns of biodiversity. PSS is available as an R package at https://github.com/cjpardodelahoz/pss .

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Species in section Peltidea (aphthosa group) of the genus Peltigera remain cryptic after molecular phylogenetic revision

Cited by 15 publications

References 67 publications

Contrasting Symbiotic Patterns in Two Closely Related Lineages of Trimembered Lichens of the Genus Peltigera

Contrasting Symbiotic Patterns in Two Closely Related Lineages of Trimembered Lichens of the Genus Peltigera

Species diversification and phylogenetically constrained symbiont switching generated high modularity in the lichen genus Peltigera

Phylogenetic structure of specialization: A new approach that integrates partner availability and phylogenetic diversity to quantify biotic specialization in ecological networks

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