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Ancient introgression drives adaptation to cooler and drier mountain habitats in a cypress species complex.

ABSTRACT: Introgression may act as an important source of new genetic variation to facilitate the adaptation of organisms to new environments, yet how introgression might enable tree species to adapt to higher latitudes and elevations remains unclear. Applying whole-transcriptome sequencing and population genetic analyses, we present an example of ancient introgression from a cypress species (Cupressus gigantea) that occurs at higher latitude and elevation on the Qinghai-Tibet Plateau into a related species (C. duclouxiana), which has likely aided the latter species to extend its range by colonizing cooler and drier mountain habitats during postglacial periods. We show that 16 introgressed candidate adaptive loci could have played pivotal roles in response to diverse stresses experienced in a high-elevation environment. Our findings provide new insights into the evolutionary history of Qinghai-Tibet Plateau plants and the importance of introgression in the adaptation of species to climate change.

SUBMITTER: Ma Y

PROVIDER: S-EPMC6581913 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Ancient introgression drives adaptation to cooler and drier mountain habitats in a cypress species complex.

Ma Yazhen Y Wang Ji J Hu Quanjun Q Li Jialiang J Sun Yongshuai Y Zhang Lei L Abbott Richard J RJ Liu Jianquan J Mao Kangshan K

Communications biology 20190618

Introgression may act as an important source of new genetic variation to facilitate the adaptation of organisms to new environments, yet how introgression might enable tree species to adapt to higher latitudes and elevations remains unclear. Applying whole-transcriptome sequencing and population genetic analyses, we present an example of ancient introgression from a cypress species (<i>Cupressus gigantea</i>) that occurs at higher latitude and elevation on the Qinghai-Tibet Plateau into a relate ...[more]

PMID: 31240251

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Project description:BackgroundAlthough the importance of host plant chemistry in plant-insect interactions is widely recognized, our understanding about the genetic basis underlying the relationship between changes in midgut proteins and adaptation of plant-feeding insects to novel host plants and habitats is very limited. To address this knowledge gap, the transcriptional profiles of midguts among three populations of the cicada Subpsaltria yangi Chen were compared. Among which, the Hancheng (HC) and Fengxiang (FX) populations occurring in the Loess Plateau feed on Ziziphus jujuba Mill. var. spinosa (Bunge) Hu ex H. F. Chow, while the population occurring in a much drier habitat in the Helan (HL) Mountains is locally specialized on a chemically divergent plant, Ephedra lepidosperma C. Y. Cheng.ResultsBased on comparative analysis, 1826 (HL vs HC) differentially expressed genes (DEGs) and 723 DEGs (HL vs FX) were identified between the populations utilizing different host plants, including 20, 36, 2, 5 and 2 genes related to digestion, detoxification, oxidation-reduction, stress response and water-deprivation response, respectively, and 35 genes presumably associated with osmoregulation. However, only 183 DEGs were identified between the HC and FX populations, including two genes related to detoxification, two genes related to stress response, and one gene presumably associated with osmoregulation. These results suggest that the weakest expression differences were between the populations utilizing the same host plant and occurring in the closest habitats, which may help explain the metabolic mechanism of adaptation in S. yangi populations to novel host plants and new niches.ConclusionsThe observed differences in gene expression among S. yangi populations are consistent with the hypothesis that the host plant shift and habitat adaptation in the HL population was facilitated by differential regulation of genes related to digestion, detoxification, oxidation-reduction, stress response, water-deprivation response and osmoregulation. The results may inform future studies on the molecular mechanisms underlying the relationship between changes in midgut proteins and adaptation of herbivorous insects to novel host plants and new niches.

Project description:Inferences about past processes of adaptation and speciation require a gene-scale and genome-wide understanding of the evolutionary history of diverging taxa. In this study, we use genome-wide capture of nuclear gene sequences, plus skimming of organellar sequences, to investigate the phylogenomics of monkeyflowers in Mimulus section Erythranthe (27 accessions from seven species). Taxa within Erythranthe, particularly the parapatric and putatively sister species M. lewisii (bee-pollinated) and M. cardinalis (hummingbird-pollinated), have been a model system for investigating the ecological genetics of speciation and adaptation for over five decades. Across >8000 nuclear loci, multiple methods resolve a predominant species tree in which M. cardinalis groups with other hummingbird-pollinated taxa (37% of gene trees), rather than being sister to M. lewisii (32% of gene trees). We independently corroborate a single evolution of hummingbird pollination syndrome in Erythranthe by demonstrating functional redundancy in genetic complementation tests of floral traits in hybrids; together, these analyses overturn a textbook case of pollination-syndrome convergence. Strong asymmetries in allele sharing (Patterson's D-statistic and related tests) indicate that gene tree discordance reflects ancient and recent introgression rather than incomplete lineage sorting. Consistent with abundant introgression blurring the history of divergence, low-recombination and adaptation-associated regions support the new species tree, while high-recombination regions generate phylogenetic evidence for sister status for M. lewisii and M. cardinalis. Population-level sampling of core taxa also revealed two instances of chloroplast capture, with Sierran M. lewisii and Southern Californian M. parishii each carrying organelle genomes nested within respective sympatric M. cardinalis clades. A recent organellar transfer from M. cardinalis, an outcrosser where selfish cytonuclear dynamics are more likely, may account for the unexpected cytoplasmic male sterility effects of selfer M. parishii organelles in hybrids with M. lewisii. Overall, our phylogenomic results reveal extensive reticulation throughout the evolutionary history of a classic monkeyflower radiation, suggesting that natural selection (re-)assembles and maintains species-diagnostic traits and barriers in the face of gene flow. Our findings further underline the challenges, even in reproductively isolated species, in distinguishing re-use of adaptive alleles from true convergence and emphasize the value of a phylogenomic framework for reconstructing the evolutionary genetics of adaptation and speciation.

Dataset Information

Ancient introgression drives adaptation to cooler and drier mountain habitats in a cypress species complex.

Publications

Ancient introgression drives adaptation to cooler and drier mountain habitats in a cypress species complex.

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