Genetic consequences of plant edaphic specialization to solfatara fields: Phylogenetic and population genetic analysis of Carex angustisquama (Cyperaceae)

Abstract

Edaphic specialization is one of the main drivers of plant diversification and has multifaceted effects on population dynamics. Carex angustisquama is a sedge plant growing only on heavily acidified soil in solfatara fields, where only extremophytes can survive. Because of the lack of closely related species in similar habitats and its disjunct distribution, the species offers ideal settings to investigate the effects of adaptation to solfatara fields and of historical biogeography on the genetic consequences of plant edaphic specialization to solfatara fields. Here, genome‐wide single nucleotide polymorphisms were used to reveal the phylogenetic origin of C. angustisquama, and 16 expressed sequence tag–simple sequence repeat markers were employed to infer population demography of C angustisquama. Molecular phylogenetic analysis strongly indicated that C. angustisquama formed a monophyletic clade with Carex doenitzii, a species growing on nonacidified soil in the sympatric subalpine zone. The result of population genetic analysis showed that C. angustisquama has much lower genetic diversity than the sister species, and notably, all 16 loci were completely homozygous in most individuals of C. angustisquama. Approximate Bayesian computation analysis supported the model that assumed hierarchical declines of population size through its evolutionary sequence. We propose that the edaphic specialist in solfatara fields has newly attained the adaptation to solfatara fields in the process of speciation. Furthermore, we found evidence of a drastic reduction in genetic diversity in C. angustisquama, suggesting that the repeated founder effects associated with edaphic specialization and subsequent population demography lead to the loss of genetic diversity of this extremophyte in solfatara fields.

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

“…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.…”

“…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.…”

Extreme low pH, not Al3+, is a key abiotic stressor for the extremophyte Carex angustisquama (Cyperaceae) in highly acidic solfatara fields

“…Although most Al in soil is insoluble and harmless to plants, the most toxic form of Al, Al 3+ is solubilized under acidic conditions (pH <5.0) (Kochian et al 2015). Because C. doenitzii is sometimes found on bare volcanic ground (Kibe & Masuzawa 1994), the ancestral species of C. angustisquama and C. doenitzii is expected to grow in the vicinity of volcanoes (Nagasawa et al 2020). Because volcanic soils are acidic with pH values occasionally below 5.0 (Delmelle et al 2015), the species might have been exposed to Al 3+ rhizotoxicity and, consequently, Al 3+ tolerance might have evolved within the ancestral species prior to the acquisition of low pH tolerance.…”

“…podocarpa (Yamamoto et al 2018) and Mimulus guttatus (Hendrick et al 2016;Kolis et al 2022)], offering a rare opportunity to investigate plant adaptive evolution in a volcanic environment. We previously examined the evolution of this unique species, which revealed that C. angustisquama forms a robust monophyletic clade with C. doenitzii Boecks., a species growing in non-acidified soil in the sympatric subalpine zone, although divergence time is unknown (Nagasawa et al 2020). Furthermore, C. angustisquama was shown to have experienced limited gene flow from closely related species with distinct habitat preferences for a long time, even though interspecific hybridizations with such species were observed (Nagasawa et al 2021a(Nagasawa et al , 2021b.…”

Genetic and reproductive characterization of distylous Primula reinii in the Hakone volcano, Japan: implications for conservation of the rare and endangered plant

“…On the other hand, the estimated effective population size in the KIN population inhabiting the somma mountains was large and constant in the long term, suggesting that the population has been maintained without suffering from volcanic eruptions occurring in the central cone. Further studies for the lineage divergence and demographic history of P. reinii in this region, using more informative datasets (e.g., single nucleotide polymorphisms), will be valuable because volcanism is one of the key abiotic factors in the plant's diversification and distribution in Japan (e.g., Yoichi et al 2017;Nagasawa et al 2020), located in the Pacific Ring of Fire.…”