Phylogeography of a widely distributed plant species reveals cryptic genetic lineages with parallel phenotypic responses to warming and drought conditions

Kahl, Sandra M.; Kappel, Christian; Joshi, Jasmin; Lenhard, Michael

doi:10.1002/ece3.8103

Cited by 9 publications

(8 citation statements)

References 123 publications

(152 reference statements)

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“…Although plants from this population share a common thermal annual phenotype with many other AH plants, they are highly differentiated genome-wide from all other populations (F ST ∼ 0.2) and showed reduced π, polymorphism, and heterozygosity despite being sampled over a similar spatial scale. Indeed, the high differentiation of AHQT in this and previous studies (Lekberg et al 2012;Hendrick et al 2016) is comparable to values for genome-wide F ST for cryptic species of Eucalyalptus and Silene recently identified at much larger spatial scales (Binks et al 2021;Kahl et al 2021). High differentiation and low diversity of AHQT also parallels that seen in a (likely selfing) solftara specialist (Nagasawa et al 2020); however, unlike that sedge and a highly selfing Agrostis grass that also colonizes our YNP thermal areas (Tercek and Whitbeck 2004), AHQT exhibits de novo mating system evolution and reproductive isolation over a scale of meters.…”

Section: Isolation In Microallopatrysupporting

confidence: 85%

Population genomic consequences of life‐history and mating system adaptation to a geothermal soil mosaic in yellow monkeyflowers

et al. 2022

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Local selection can promote phenotypic divergence despite gene flow across habitat mosaics, but adaptation itself may generate substantial barriers to genetic exchange. In plants, life-history, phenology, and mating system divergence have been proposed to promote genetic differentiation in sympatry. In this study, we investigate phenotypic and genetic variation in Mimulus guttatus (yellow monkeyflowers) across a geothermal soil mosaic in Yellowstone National Park (YNP). Plants from thermal annual and nonthermal perennial habitats were heritably differentiated for life-history and mating system traits, consistent with local adaptation to the ephemeral thermal-soil growing season. However, genome-wide genetic variation primarily clustered plants by geographic region, with little variation sorting by habitat. The one exception was an extreme thermal population also isolated by a 200 m geographical gap of no intermediate habitat. Individual inbreeding coefficients (F IS ) were higher (and predicted by trait variation) in annual plants and annual pairs showed greater isolation by distance at local (<1 km) scales. Finally, YNP adaptation does not reuse a widespread inversion that underlies M. guttatus life-history ecotypes range-wide, suggesting a novel genetic mechanism. Overall, this work suggests that life-history and mating system adaptation strong enough to shape individual mating patterns does not necessarily generate incipient speciation without geographical barriers.

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Section: Isolation In Microallopatrysupporting

confidence: 85%

Population genomic consequences of life‐history and mating system adaptation to a geothermal soil mosaic in yellow monkeyflowers

et al. 2022

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“…We attribute this observed divergence to E. nutans ’ wider ecological niche and larger effective population size, which likely enhance individuals’ migration and dispersion across diverse habitats, facilitating gene flow among populations. Such occurrences are common among widely distributed plant species and are pivotal in maintaining genetic diversity and adaptability within populations ( Broadhurst et al., 2018 ; Kahl et al., 2021 ; Veto et al., 2023 ).…”

Section: Discussionmentioning

confidence: 99%

Phylogeographic analysis reveals extensive genetic variation of native grass Elymus nutans (Poaceae) on the Qinghai-Tibetan plateau

Li,

Zhang

et al. 2024

Front. Plant Sci.

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IntroductionElymus nutans holds ecological and pastoral significance due to its adaptability and nutritional value, the Qinghai-Tibet Plateau (QTP) is a key hub for its genetic diversity. To conserve and harness its genetic resources in highland ecosystems, a thorough assessment is vital. However, a comprehensive phylogeographic exploration of E. nutans is lacking. The objective of this study was to unravel the genetic diversity, adaptation, and phylogenetics of E. nutans populations.MethodsEncompassing 361 individuals across 35 populations, the species' genetic landscape and dynamic responses to diverse environments were decoded by using four chloroplast DNA (cpDNA) sequences and nine microsatellite markers derived from the transcriptome.Results and discussionThis study unveiled a notable degree of genetic diversity in E. nutans populations at nuclear (I = 0.46, He = 0.32) and plastid DNA levels (Hd = 0.805, π = 0.67). Analysis via AMOVA highlighted genetic variation predominantly within populations. Despite limited isolation by distance (IBD), the Mekong-Salween Divide (MSD) emerged as a significant factor influencing genetic differentiation and conserving diversity. Furthermore, correlations were established between external environmental factors and effective alleles of three EST-SSRs (EN5, EN57 and EN80), potentially linked to glutathione S-transferases T1 or hypothetical proteins, affecting adaptation. This study deepens the understanding of the intricate relationship between genetic diversity, adaptation, and environmental factors within E. nutans populations on the QTP. The findings shed light on the species' evolutionary responses to diverse ecological conditions and contribute to a broader comprehension of plant adaptation mechanisms.

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“…Understanding the origin and maintenance of intraspecific variation is of central importance to evolutionary biology because they inform our understanding of diversification across space and time and illuminate the process of speciation (Pinheiro et al, 2018). Substantial intraspecific phenotypic variation may indicate the maintenance of polymorphisms over otherwise connected populations (Nobarinezhad and Wallace, 2022), or it could indicate the presence of evolutionarily divergent cryptic lineages that exhibit parallel ecological responses (Kahl et al, 2021). Whereas a polymorphic species is expected to experience spatially and temporally heterogeneous gene flow among populations, cryptic lineages exhibiting genetic divergence should be isolated from one another (Surveswaran et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

Floral and genetic divergence across environmental gradients is moderated by inter-population gene flow in Platanthera dilatata (Orchidaceae)

Wallace

Bowles

2023

Front. Ecol. Evol.

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Understanding how natural selection acts on intraspecific variation to bring about phenotypic divergence is critical to understanding processes of evolutionary diversification. The orchid family is well known for pollinator-mediated selection of floral phenotypes operating among species and along environmental or geographic gradients. Its effectiveness at small spatial scales is less understood, making the geographic scale at which intraspecific floral variation is examined important to evaluating causes of phenotypic divergence. In this study, we quantified phenotypic variation in the orchid Platanthera dilatata across 26 populations in coastal Southeast Alaska and compared this to edaphic and genetic variation at microsatellite loci. We sought to determine (1) if flower morphological variation is structured at smaller geographic scales, (2) the extent of genetic divergence in relation to phenotypic divergence, (3) the scale at which inter-population gene flow occurs, and (4) the relative importance of geographic distance and abiotic factors on population genetic structure. Two morphological groups were found to separate based on lip and spur length and are restricted to different habitats. Small-flowered forms occur in muskeg bogs, whereas large-flowered forms occur in fens and meadows, and rarely in sub-alpine habitat. Genetic analyses were concordant with the morphological clusters, except for four small-flowered populations that were genetically indistinguishable from large-flowered populations and considered to be introgressed. In fact, most populations exhibited some admixture, indicating incomplete reproductive isolation between the flower forms. Pollinators may partition phenotypes but also facilitate gene flow because short-tongued Noctuidae moths pollinate both phenotypes, but longer-tongued hawkmoths were only observed pollinating the large-flowered phenotype, which may strengthen phenotypic divergence. Nevertheless, pollinator movement between habitats could have lasting effects on neutral genetic variation. At this small spatial scale, population genetic structure is only associated with environmental distance, likely due to extensive seed and pollinator movement. While this study corroborates previous findings of cryptic genetic lineages and phenotypic divergence in P. dilatata, the small scale of examination provided greater understanding of the factors that may underlie divergence.

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Phylogeography of a widely distributed plant species reveals cryptic genetic lineages with parallel phenotypic responses to warming and drought conditions

Abstract: This is an open access article under the terms of the Creat ive Commo ns Attri bution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Cited by 9 publications

References 123 publications

Population genomic consequences of life‐history and mating system adaptation to a geothermal soil mosaic in yellow monkeyflowers

Population genomic consequences of life‐history and mating system adaptation to a geothermal soil mosaic in yellow monkeyflowers

Phylogeographic analysis reveals extensive genetic variation of native grass Elymus nutans (Poaceae) on the Qinghai-Tibetan plateau

Floral and genetic divergence across environmental gradients is moderated by inter-population gene flow in Platanthera dilatata (Orchidaceae)

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