Lineage and role in integrative taxonomy of a heterotrophic orchid complex

Abstract

Lineage‐based species definitions applying coalescent approaches to species delimitation have become increasingly popular. Yet, the application of these methods and the recognition of lineage‐only definitions have recently been questioned. Species delimitation criteria that explicitly consider both lineages and evidence for ecological role shifts provide an opportunity to incorporate ecologically meaningful data from multiple sources in studies of species boundaries. Here, such criteria were applied to a problematic group of mycoheterotrophic orchids, the Corallorhiza striata complex, analysing genomic, morphological, phenological, reproductive‐mode, niche, and fungal host data. A recently developed method for generating genomic polymorphism data–ISSRseq–demonstrates evidence for four distinct lineages, including a previously unidentified lineage in the Coast Ranges and Cascades of California and Oregon, USA. There is divergence in morphology, phenology, reproductive mode, and fungal associates among the four lineages. Integrative analyses, conducted in population assignment and redundancy analysis frameworks, provide evidence of distinct genomic lineages and a similar pattern of divergence in the extended data, albeit with weaker signal. However, none of the extended data sets fully satisfy the condition of a significant role shift, which requires evidence of fixed differences. The four lineages identified in the current study are recognized at the level of variety, short of comprising different species. This study represents the most comprehensive application of lineage + role to date and illustrates the advantages of such an approach.

Monotropastrum kirishimense (Ericaceae), a new mycoheterotrophic plant from Japan based on multifaceted evidence

“…Furthermore, speciation between Monotropastrum kirishimense and M. humile may be partially due to resource partitioning, with specialization on different fungal hosts leading to reproductive isolation (see also Barrett and Freudenstein 2011 ; Barrett et al 2022 ). Speciation via host shift is one of the most plausible modes of ecological speciation (Calcagno et al 2007 ; Fry 2003 ).…”

“…Hybridization between ecotypes within a single mycoheterotrophic species with different host specificity can considerably reduce progeny fitness due to a lower probability of mycoheterotrophic growth (Jacquemyn et al 2016 , 2018 ). Consequently, differences in mycorrhizal communities have been suggested to contribute to reproductive isolation among mycoheterotrophic plants (Barrett and Freudenstein 2011 ; Barrett et al 2022 ; Jacquemyn et al 2018 ). Future investigations, including artificial interspecific cross-pollination experiments and in-situ seed baiting, are required to determine whether mycorrhizal associations can prevent hybrid seeds from establishing successful seedlings, thus acting as a post-mating barrier in these two Monotropastrum species.…”

“…We then reconstructed the phylogenetic relationships to examine whether the taxon represents distinct evolutionary lineages, based on MIG-seq [multiplexed inter-simple sequence repeat (ISSR) genotyping by sequencing] data. Finally, given that fungal-associate identity may be relevant in delimiting mycoheterotrophic taxa (Barrett and Freudenstein 2011 ; Barrett et al 2022 ; Freudenstein and Barrett 2014 ), we investigated the mycorrhizal fungal communities of this taxon and M. humile , including at a sympatric site, using high-throughput DNA sequencing. Our multifaceted evidence leads us to conclude that this taxon is morphologically, phenologically, phylogenetically, and ecologically distinct, and should, therefore, be recognized as a separate species.…”

Spiranthes hachijoensis (Orchidaceae), a new species within the S. sinensis species complex in Japan, based on morphological, phylogenetic, and ecological evidence

“…Species delimitation that explicitly considers ecological and phylogenetic differences has critically advanced the current understanding and evaluation of biodiversity (Barrett and Freudenstein 2011 ). Over the last two decades, these integrative taxonomic approaches have provided more robust estimates of biodiversity among taxonomically challenging species (Barrett and Freudenstein 2011 ; Barrett et al 2022 ; Botes et al 2020 ; Pace et al 2019 ; Suetsugu et al 2023 ). The present study provides morphological, phylogenetic, and ecological evidence that supports the recognition of S. hachijoensis Suetsugu, named after its type locality, which sustains the largest population of the taxon.…”

Morphological, ecological, and molecular phylogenetic approaches reveal species boundaries and evolutionary history of Goodyera crassifolia (Orchidaceae, Orchidoideae) and its closely related taxa

“…Species delimitation that explicitly considers ecological as well as phylogenetic differences represents a crucial step in our understanding of biodiversity ( Barrett and Freudenstein 2011 ). Over the last two decades, integrative taxonomy has helped achieve more robust estimates of biodiversity than those based on one-dimensional representations of variation (such as morphology), especially in the case of taxonomically challenging species ( Barrett and Freudenstein 2011 ; Botes et al 2020 ; Barrett et al 2022 ). Our multifaceted evidence leads us to conclude that G. crassifolia is morphologically, phylogenetically, and ecologically distinct from G. schlechtendaliana and G. × tamnaensis and should, therefore, be considered as a separate species.…”