Coalescent-Based Species Delimitation Approach Uncovers High Cryptic Diversity in the Cosmopolitan Lichen-Forming Fungal Genus Protoparmelia (Lecanorales, Ascomycota)

Singh, Garima; Grande, Francesco Dal; Divakar, Pradeep K.; Juergen, Otte; Leavitt, Steven D.; Szczepańska, Katarzyna; Crespo, Ana; Rico, Vı́ctor J.; Aptroot, André; Cáceres, Marcela Eugenia da Silva; Lumbsch, H. Thorsten; Schmitt, Imke

doi:10.1371/journal.pone.0124625

Cited by 67 publications

(84 citation statements)

References 76 publications

(101 reference statements)

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“…The addition of extra samples to the published fungal phylogeny did not change the topology of the fungal tree and the concatenated fungal tree is concordant with Singh et al . (; Fig. S6).…”

Section: Resultsmentioning

confidence: 97%

Fungal–algal association patterns in lichen symbiosis linked to macroclimate

et al. 2016

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Both macroclimate and evolutionary events may influence symbiont association and diversity patterns. Here we assess how climatic factors and evolutionary events shape fungal-algal association patterns in the widely distributed lichen-forming fungal genus Protoparmelia. Multilocus phylogenies of fungal and algal partners were generated using 174 specimens. Coalescent-based species delimitation analysis suggested that 23 fungal hosts are associating with 20 algal species. Principal component analysis (PCA) was performed to infer how fungal-algal association patterns varied with climate. Fungi associated with one to three algal partners whereas algae accepted one to five fungal partners. Both fungi and algae were more specific, associating with fewer partners, in the warmer climates. Interaction with more than one partner was more frequent in cooler climates for both the partners. Cophylogenetic analyses suggest congruent fungal-algal phylogenies. Host switch was a more common event in warm climates, whereas failure of the photobiont to diverge with its fungal host was more frequent in cooler climates. We conclude that both environmental factors and evolutionary events drive fungal and algal evolution in Protoparmelia. The processes leading to phylogenetic congruence of fungi and algae are different in different macrohabitats in our study system. Hence, closely related species inhabiting diverse habitats may follow different evolutionary pathways.

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Section: Resultsmentioning

confidence: 97%

Fungal–algal association patterns in lichen symbiosis linked to macroclimate

et al. 2016

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“…The same general pattern, with variations on the theme, repeats itself in rock‐dwelling species of Protoparmelia (Singh et al . ), within Tephromela (Muggia et al . ), and within the Sarcogyne – Acarospora complex (Westberg et al .…”

Section: Discussionmentioning

confidence: 99%

“…; Singh et al . ). Few explanations have been proffered as to what mechanisms give rise to cryptic speciation in the absence of visible phenotypes on which natural selection could act.…”

Section: Introductionmentioning

confidence: 97%

Escape from the cryptic species trap: lichen evolution on both sides of a cyanobacterial acquisition event

2016

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Large, architecturally complex lichen symbioses arose only a few times in evolution, increasing thallus size by orders of magnitude over those from which they evolved. The innovations that enabled symbiotic assemblages to acquire and maintain large sizes are unknown. We mapped morphometric data against an eight‐locus fungal phylogeny across one of the best‐sampled thallus size transition events, the origins of the Placopsis lichen symbiosis, and used a phylogenetic comparative framework to explore the role of nitrogen‐fixing cyanobacteria in size differences. Thallus thickness increased by >150% and fruiting body core volume increased ninefold on average after acquisition of cyanobacteria. Volume of cyanobacteria‐containing structures (cephalodia), once acquired, correlates with thallus thickness in both phylogenetic generalized least squares and phylogenetic generalized linear mixed‐effects analyses. Our results suggest that the availability of nitrogen is an important factor in the formation of large thalli. Cyanobacterial symbiosis appears to have enabled lichens to overcome size constraints in oligotrophic environments such as acidic, rain‐washed rock surfaces. In the case of the Placopsis fungal symbiont, this has led to an adaptive radiation of more than 60 recognized species from related crustose members of the genus Trapelia. Our data suggest that precyanobacterial symbiotic lineages were constrained to forming a narrow range of phenotypes, so‐called cryptic species, leading systematists until now to recognize only six of the 13 species clusters we identified in Trapelia.

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“…Coalescent theory is now being widely applied to empirically delimit species and many methods are available (Fujita et al ., ). In lichenized fungi the use of coalescent‐based methods has been widely used to delimit species (Parnmen et al ., ; Leavitt et al ., , ; Saag et al ., ; Kraichak et al ., ; Leavitt, Moreau & Lumbsch, ; Singh et al ., ).…”

Section: Introductionmentioning

confidence: 97%

“…During the past decade, there has been an increased interest in integrative species delimitation that combines multiple lines of evidence (Sites & Marshall, ; Padial et al ., ). Integrating traditional morphological data with molecular data, however, can be challenging due to a number of issues such as the presence of cryptic species (Bickford et al ., ; Leavitt et al ., ; Singh et al ., ) and effects of adaptive radiations (Shaffer & Thomson, ; Maddison, ). Traditional phenotype‐based methods may fail to detect species boundaries in cryptic lineages, resulting in an underestimate of the true number of species relative to other kinds of data (Bickford et al ., ).…”

Section: Introductionmentioning

confidence: 99%

Picking holes in traditional species delimitations: an integrative taxonomic reassessment of theParmotrema perforatumgroup (Parmeliaceae, Ascomycota)

et al. 2016

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Accurate species delimitation is important as species are a fundamental unit in ecological, evolutionary and conservation biology research. In lichenized fungi, species delimitation has been difficult due to a lack of taxonomically important characteristics and due to the limits of traditional, morphology‐based species concepts. In this study we reassess the current taxonomy of the Parmotrema perforatum group, which recognizes six closely related species divided into three species pairs, each pair comprising one apotheciate (sexual) and one sorediate (asexual) species. Each pair is further characterized by a distinct combination of secondary metabolites. It was hypothesized that the three apotheciate species are reproductively isolated sibling species and that each sorediate species evolved once from the chemically identical apotheciate species. In this study, species boundaries were re‐examined using an integrative approach incorporating morphological, chemical and molecular sequence data to delimit species boundaries. Phylogenetic trees were inferred from a seven‐locus DNA sequence dataset using concatenated gene tree and coalescent‐based species‐tree inference methods. Furthermore, we employed a multi‐species coalescent method to validate candidate species. Micromorphological measurements of conidia were found to be congruent with phylogenetic clusters. Each approach that we applied to the P. perforatum group consistently recovered four of the currently circumscribed species (P. perforatum, P. hypotropum, P. subrigidum and P. louisianae), whereas P. preperforatum and P. hypoleucinum were consistently combined and are thus interpreted as conspecific.

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Coalescent-Based Species Delimitation Approach Uncovers High Cryptic Diversity in the Cosmopolitan Lichen-Forming Fungal Genus Protoparmelia (Lecanorales, Ascomycota)

Cited by 67 publications

References 76 publications

Fungal–algal association patterns in lichen symbiosis linked to macroclimate

Fungal–algal association patterns in lichen symbiosis linked to macroclimate

Escape from the cryptic species trap: lichen evolution on both sides of a cyanobacterial acquisition event

Picking holes in traditional species delimitations: an integrative taxonomic reassessment of theParmotrema perforatumgroup (Parmeliaceae, Ascomycota)

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