skip to main content


Title: The Sticta filix - Sticta lacera conundrum (lichenized Ascomycota: Peltigeraceae subfamily Lobarioideae): unresolved lineage sorting or developmental switch?
Abstract

We assessed the status of two New Zealand endemic morphodemes in the genus Sticta, currently treated as two separate taxa, Sticta filix and Sticta lacera. Both are green-algal lichens with a distinct stipe that grow in forested habitats and are suitable indicators of the indigenous vegetation health in forest ecosystems in New Zealand. They exhibit different morphologies and substrate ecologies: S. filix forms rather robust thalli, often on exposed trunks of phorophytes, with erect stems distinctly emerging from the substrate, whereas S. lacera is a more delicate lichen growing near the base of trees, usually among bryophyte mats or sheltered in the exposed portions of the phorophyte root-plate, with a prostrate, branched, stolon-like stem barely emerging from the substrate. Throughout their range, both taxa grow sympatrically and often in close proximity (syntopically). Despite the differences, ITS barcoding does not support the two morphodemes as separate species. In this study we assessed two possible explanations: (1) S. filix and S. lacera are discrete phenotypes of a single species, caused by developmental switching triggered by a discrete environmental variable, the propagules developing either on bare substrate or between bryophytes; and (2) the two morphodemes represent separate lineages, but ITS does not provide sufficient resolution to reflect this. We performed a quantitative analysis of morphological and ecological parameters, based on vouchered herbarium collections and field observations on iNaturalist NZ (https://inaturalist.nz), to assess the level of discreteness of the growth forms and to test for a correlation with the presence of a bryophyte mat. We further took advantage of an existing molecular data set from a target capture approach, comprised of 205 protein markers. This data set was used to establish a framework of percentage identities between pairs of the same and of different species among lobarioid Peltigeraceae and then to test whether the S. filix/lacera pairing fell closer to a within-species or a between-species pairing. The morphometric analysis of herbarium material resolved S. filix and S. lacera as two discrete morphs with little overlap, supported by numerous observations on iNaturalist NZ. However, whereas herbarium material suggested a significant association of the lacera morph with bryophyte mats, no such pattern was evident from field images on iNaturalist NZ, in which both morphs frequently associated with bryophyte mats. This highlights the limitations of herbarium material to correctly assess substrate ecology, whereas iNaturalist NZ postings had issues with correct identifications, given that especially S. lacera is easily confused with Pseudocyphellaria multifida. Based on the target capture data, the percentage identity of the S. filix/lacera pairing (99.43%) was significantly higher than that of all 12 between-species pairings (93.20–98.01%); it was at the same time lower than that of all within-species pairings (99.63–99.99%) but significantly so only in comparison with five out of the eight within-species pairings. The target capture approach is thus inconclusive, but the combination of all data suggests that S. filix and S. lacera are not discrete morphodemes of a single species but represent two separate lineages which emerged recently and hence cannot be resolved using the ITS barcoding marker or even a deeper phylogenomic approach based on protein-coding markers. We propose transplantation experiments and the application of RADseq to further assess this situation.

 
more » « less
NSF-PAR ID:
10386984
Author(s) / Creator(s):
; ; ; ; ;
Publisher / Repository:
Oxford University Press
Date Published:
Journal Name:
Botanical Journal of the Linnean Society
Volume:
199
Issue:
3
ISSN:
0024-4074
Format(s):
Medium: X Size: p. 706-727
Size(s):
["p. 706-727"]
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Accurate species delimitations are fundamental to our understanding of the genetic diversity on Earth and a vital part in evolutionary and conservation biology research. In lichenized fungi, species pairs have the same morphology and chemistry. They only differ in how they reproduce with one species using sexual reproductive structures and the other using asexual propagules. To classify these as one species or two has been a point of contention, and conclusions based on Sanger sequencing, where sequence data are limited and species boundaries are usually not observed, have been refuted after analysis with genome-scale data such as restriction site-associated DNA sequencing that tends to find fixed genetic differences between the two morphs. Pseudocyphellaria glabra and P. homoeophylla have long been considered a species pair that differ in geographical ranges but co-occur in New Zealand. We used restriction site-associated DNA sequencing data and generated thousands of genetic loci across 53 individuals. The RADseq data provided high-resolution phylogenetic and population genomic information. A maximum-likelihood phylogenetic reconstruction recovered both species as separate lineages, whereas population genetics indicated some evidence for admixture among P. glabra and P. homoeophylla from New Zealand. It is not clear whether the latter is due to ancient polymorphism or recent gene flow. Our study represents another example of the usefulness of RADseq to test species boundaries that segregate closely related species in lichenized fungi.

     
    more » « less
  2. Abstract Aim

    Phylogenetic diversification is a precursor to speciation, but the underlying patterns and processes are not well‐studied in lichens. Here we investigate what factors drive diversification in two tropical, morphologically similar macrolichens that occupy a similar range but differ in altitudinal and habitat preferences, testing for isolation by distance (IBD), environment (IBE), and fragmentation (IBF).

    Location

    Neotropics, Hawaii, Macaronesia.

    Taxon

    Sticta andina,S. scabrosa(Peltigeraceae).

    Methods

    We analysed 395 specimens from 135 localities, using the fungal ITS barcoding marker to assess phylogenetic diversification, through maximum likelihood tree reconstruction, TCS haplotype networks, and Tajima's D. Mantel tests were employed to detect structure in genetic vs. geographic, environmental, and fragmentation distances. Habitat preferences were quantitatively assessed by statistical analysis of locality‐based BIOclim variables.

    Results

    Sticta andinaexhibited high phenotypic variation and reticulate phylogenetic diversity across its range, whereas the phenotypically uniformS. scabrosacontained two main haplotypes, one unique to Hawaii.Sticta andinais restricted to well‐preserved andine forests and paramos, naturally fragmented habitats due to disruptive topology, whereasS. scabrosathrives in lowland to lower montane zones in exposed or disturbed microsites, representing a continuous habitat.Sticta scabrosashowed IBD only across its full range (separating the Hawaiian population) but not within continental Central and South America, there exhibiting a negative Tajima's D.Sticta andinadid not exhibit IBD but IBE at continental level and IBF in the northern Andes.

    Main conclusions

    Autecology, particularly preference for either low or high altitudes, indirectly drives phylogenetic diversification. Low diversification in the low altitude species,S. scabrosa, can be attributed to rapid expansion and effective gene flow across a more or less continuous niche due to disturbance tolerance. In contract, high diversification in the high altitude species,S. andina, can be explained by niche differentiation (IBE) and fragmentation (IBF) caused by the Andean uplift.

     
    more » « less
  3. Abstract— Like many fern lineages comprising reticulate species complexes, Polypodium s.s. (Polypodiacaeae) has a history shaped by rapid diversification, hybridization, and polyploidy that poses substantial challenges for phylogenetic inference with plastid and single-locus nuclear markers. Using target capture probes for 408 nuclear loci developed by the GoFlag project and a custom bioinformatic pipeline, SORTER, we constructed multi-locus nuclear datasets for diploid temperate and Mesoamerican species of Polypodium and five allotetraploid species belonging to the well-studied Polypodium vulgare complex. SORTER employs a clustering approach to separate putatively paralogous copies of targeted loci into orthologous matrices and haplotype phasing to infer allopolyploid haplotypes across loci, resulting in datasets amenable to both concatenated maximum likelihood and multi-species coalescent phylogenetic analyses. By comparing phylogenies derived from maximum likelihood and multi-species coalescent analyses of unphased and phased datasets, as well as evaluating discordance among gene trees and species trees, we recover support for incomplete lineage sorting within Polypodium s.s., novel relationships among diploid taxa of the Polypodium vulgare complex and its Mesoamerican sister clade, and the placement of several Polypodium species within other genera. Additionally, we were able to infer well-supported phylogenies that identified the hypothesized progenitors of the allotetraploid species, indicating that SORTER is an effective and accurate tool for reconstructing homeolog haplotypes of allopolyploids in fern taxa and other non-model organisms from target capture data. 
    more » « less
  4. The Opiliones family Neopilionidae is restricted to the terranes of the former temperate Gondwana: South America, Africa, Australia, New Caledonia and New Zealand. Despite decades of morphological study of this unique fauna, it has been difficult reconciling the classic species of the group (some described over a century ago) with recent cladistic morphological work and previous molecular work. Here we attempted to investigate the pattern and timing of diversification of Neopilionidae by sampling across the distribution range of the family and sequencing three markers commonly used in Sanger-based approaches (18S rRNA, 28S rRNA and cytochrome-c oxidase subunit I). We recovered a well-supported and stable clade including Ballarra (an Australian ballarrine) and the Enantiobuninae from South America, Australia, New Caledonia and New Zealand, but excluding Vibone (a ballarrine from South Africa). We further found a division between West and East Gondwana, with the South American Thrasychirus/Thrasychiroides always being sister group to an Australian–Zealandian (i.e. Australia + New Zealand + New Caledonia) clade. Resolution of the Australian–Zealandian taxa was analysis-dependent, but some analyses found Martensopsalis, from New Caledonia, as the sister group to an Australian–New Zealand clade. Likewise, the species from New Zealand formed a clade in some analyses, but Mangatangi often came out as a separate lineage from the remaining species. However, the Australian taxa never constituted a monophyletic group, with Ballarra always segregating from the remaining Australian species, which in turn constituted 1–3 clades, depending on the analysis. Our results identify several generic inconsistencies, including the possibility of Thrasychiroides nested within Thrasychirus, Forsteropsalis being paraphyletic with respect to Pantopsalis, and multiple lineages of Megalopsalis in Australia. In addition, the New Zealand Megalopsalis need generic reassignment: Megalopsalis triascuta will require its own genus and M. turneri is here transferred to Forsteropsalis, as Forsteropsalis turneri (Marples, 1944), comb. nov. 
    more » « less
  5. Abstract

    As coral populations decline worldwide in the face of ongoing environmental change, documenting their distribution, diversity and conservation status is now more imperative than ever. Accurate delimitation and identification of species is a critical first step. This task, however, is not trivial as morphological variation and slowly evolving molecular markers confound species identification. New approaches to species delimitation in corals are needed to overcome these challenges. Here, we test whether target enrichment of ultraconserved elements (UCEs) and exons can be used for delimiting species boundaries and population structure within species of corals by focusing on two octocoral genera,AlcyoniumandSinularia, as exemplary case studies. We designed an updated bait set (29,181 baits) to target‐capture 3,023 UCE and exon loci, recovering a mean of 1,910 ± 168SDper sample with a mean length of 1,055 ± 208 bp. Similar numbers of loci were recovered fromSinularia(1,946 ± 227SD) andAlcyonium(1,863 ± 177SD). Species‐level phylogenies were highly supported for both genera. Clustering methods based on filtered single nucleotide polymorphisms delimited species and populations that are congruent with previous allozyme, DNA barcoding, reproductive and ecological data forAlcyonium, and offered further evidence of hybridization among species. ForSinularia, results were congruent with those obtained from a previous study using restriction site associated DNA sequencing. Both case studies demonstrate the utility of target‐enrichment of UCEs and exons to address a wide range of evolutionary and taxonomic questions across deep to shallow timescales in corals.

     
    more » « less