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Adaptive divergence generates distinct plastic responses in two closely related Senecio species.

ABSTRACT: The evolution of plastic responses to external cues allows species to maintain fitness in response to the environmental variations they regularly experience. However, it remains unclear how plasticity evolves during adaptation. To test whether distinct patterns of plasticity are associated with adaptive divergence, we quantified plasticity for two closely related but ecologically divergent Sicilian daisy species (Senecio, Asteraceae). We sampled 40 representative genotypes of each species from their native range on Mt. Etna and then reciprocally transplanted multiple clones of each genotype into four field sites along an elevational gradient that included the native elevational range of each species, and two intermediate elevations. At each elevation, we quantified survival and measured leaf traits that included investment (specific leaf area), morphology, chlorophyll fluorescence, pigment content, and gene expression. Traits and differentially expressed genes that changed with elevation in one species often showed little changes in the other species, or changed in the opposite direction. As evidence of adaptive divergence, both species performed better at their native site and better than the species from the other habitat. Adaptive divergence is, therefore, associated with the evolution of distinct plastic responses to environmental variation, despite these two species sharing a recent common ancestor.

SUBMITTER: Walter GM

PROVIDER: S-EPMC9322604 | biostudies-literature | 2022 Jun

REPOSITORIES: biostudies-literature

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Adaptive divergence generates distinct plastic responses in two closely related Senecio species.

Walter Greg M GM Clark James J Cristaudo Antonia A Terranova Delia D Nevado Bruno B Catara Stefania S Paunov Momchil M Velikova Violeta V Filatov Dmitry D Cozzolino Salvatore S Hiscock Simon J SJ Bridle Jon R JR

Evolution; international journal of organic evolution 20220418 6

The evolution of plastic responses to external cues allows species to maintain fitness in response to the environmental variations they regularly experience. However, it remains unclear how plasticity evolves during adaptation. To test whether distinct patterns of plasticity are associated with adaptive divergence, we quantified plasticity for two closely related but ecologically divergent Sicilian daisy species (Senecio, Asteraceae). We sampled 40 representative genotypes of each species from t ...[more]

PMID: 35344205

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Project description:BackgroundDivergent genetic responses to the same environmental pressures may lead sympatric ecological speciation possible. Such speciation process possibly explains rapid sympatric speciation of island species. Two island endemic ginger species Zingiber kawagoii and Z. shuanglongensis was suggested to be independently originated from inland ancestors, but their island endemism and similar morphologies and habitats lead another hypothesis of in situ ecological speciation. For understanding when and how these two species diverged, intraspecific variation was estimated from three chloroplast DNA fragments (cpDNA) and interspecific genome-wide SNPs and expression differences after saline treatment were examined by transcriptomic analyses.ResultsExtremely low intraspecific genetic variation was estimated by cpDNA sequences in both species: nucleotide diversity π = 0.00002 in Z. kawagoii and no nucleotide substitution but only indels found in Z. shuanglongensis. Nonsignificant inter-population genetic differentiation suggests homogenized genetic variation within species. Based on 53,683 SNPs from 13,842 polymorphic transcripts, in which 10,693 SNPs are fixed between species, Z. kawagoii and Z. shuanglongensis were estimated to be diverged since 218~ 238 thousand generations ago (complete divergence since 41.5~ 43.5 thousand generations ago). This time is more recent than the time of Taiwan Island formation. In addition, high proportion of differential expression genes (DEGs) is non-polymorphic or non-positively selected, suggesting key roles of plastic genetic divergence in broaden the selectability in incipient speciation. While some positive selected DEGs were mainly the biotic and abiotic stress-resistance genes, emphasizing the importance of adaptive divergence of stress-related genes in sympatric ecological speciation. Furthermore, the higher proportional expression of functional classes in Z. kawagoii than in Z. shuanglongensis explains the more widespread distribution of Z. kawagoii in Taiwan.ConclusionsOur results contradict the previous hypothesis of independent origination of these two island endemic ginger species from SE China and SW China. Adaptive divergent responses to the stress explain how these gingers maintain genetic differentiation in sympatry. However, the recent speciation and rapid expansion make extremely low intraspecific genetic variation in these two species. This study arise a more probable speciation hypothesis of sympatric speciation within an island via the mutation-order mechanism underlying the same environmental pressure.

Project description:Ecological speciation is a common mechanism by which new species arise. Despite great efforts, the role of gene expression in ecological divergence and speciation is poorly understood. Here, we conducted a genome-wide gene expression investigation of two Oryza species that are evolutionarily young and distinct in ecology and morphology. Using digital gene expression (DGE) technology and the paired-end RNA sequencing (RNA-Seq) method, we obtained 21,415 expressed genes across three reproduction-related tissues at two critical developmental stages. Of them, ~8% (1717) differed significantly in expression levels between the two species and these differentially expressed genes are randomly distributed across the genome. Moreover, 62% (1064) of the differentially expressed genes exhibited a signature of directional selection in at least one species. Importantly, the genes with differential expression between species evolved more rapidly at the 5â??flanking sequences than the genes without differential expression relative to coding sequences, suggesting that cis-regulatory changes are likely adaptive and play an important role in the ecological divergence of the two species. Finally, we showed evidence of significant differentiation between species in phenotype traits and observed that genes with differential expression were overrepresented with functional terms involving phenotypic and ecological differentiation between the two species, including reproduction- and stress-related characteristics. Our findings demonstrate that ecological speciation is associated with widespread and adaptive alterations in genome-wide gene expression and highlight the dominant role of regulatory evolution in ecological divergence and adaptation. We selected accessions representing typical Oryza rufipogon and O. nivara, which were sampled exclusively from South and Southeast Asia where the two species overlap. We chose to collect three types of tissues, i.e., flag leaves at the heading stage (2â??7 cm above the primary branch) (L), panicles at the heading stage (H) and panicles at the flowering stage (10â??15 cm above the primary branch) (F). Sample collection was repeated twice in two consecutive years (2009 and 2010) under the same controlled conditions. A total of 36 samples were sequenced by Illuminaâ??s digital gene expression (DGE) system, with each type of tissues collected from six individuals of each species as biological replicates. To access the quality of DGE technology, we also selected six samples representing three tissues from each of two individuals (one individual per species) for paired-end RNA-Seq sequencing.

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Adaptive divergence generates distinct plastic responses in two closely related Senecio species.

Publications

Adaptive divergence generates distinct plastic responses in two closely related Senecio species.

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