Localized environmental heterogeneity drives the population differentiation of two endangered and endemic Opisthopappus Shih species

Abstract

Background Climate heterogeneity not only indirectly shapes the genetic structures of plant populations, but also drives adaptive divergence by impacting demographic dynamics. The variable localized climates and topographic complexity of the Taihang Mountains make them a major natural boundary in Northern China that influences the divergence of organisms distributed across this region. Opisthopappus is an endemic genus of the Taihang Mountains that includes only two spatially partitioned species Opisthopappus longilobus and Opisthopappus taihangensis. For this study, the mechanisms behind the genetic variations in Opisthopappus populations were investigated. Results Using SNP and InDel data coupled with geographic and climatic information, significant genetic differentiation was found to exist either between Opisthopappus populations or two species. All studied populations were divided into two genetic groups with the differentiation of haplotypes between the groups. At approximately 17.44 Ma of the early Miocene, O. taihangensis differentiated from O. longilobus under differing precipitation regimes due to the intensification of the Asian monsoon. Subsequently, intraspecific divergence might be induced by the dramatic climatic transformation from the mid- to late Miocene. During the Pleistocene period, the rapid uplift of the Taihang Mountains coupled with violent climatic oscillations would further promote the diversity of the two species. Following the development of the Taihang Mountains, its complex topography created geographical and ecological heterogeneity, which could lead to spatiotemporal isolation between the Opisthopappus populations. Thus the adaptive divergence might occur within these intraspecific populations in the localized heterogeneous environment of the Taihang Mountains. Conclusions The localized environmental events through the integration of small-scale spatial effects impacted the demographic history and differentiation mechanism of Opisthopappus species in the Taihang Mountains. The results provide useful information for us to understand the ecology and evolution of organisms in the mountainous environment from population and species perspective.

Adaptation insights from comparative transcriptome analysis of two Opisthopappus species in the Taihang mountains

“…Previous studies have confirmed significant differentiation and variation between O. longilobus and O. taihangensis based on geographic distribution, morphological characteristics and DNA information [ 26 , 27 , 29 – 33 ]. Subsequently, Chai [ 28 , 34 ] used transcriptome data to reveal differentially expressed genes and screened DNA markers of the two species to further prove the differentiation and variation between the two species.…”

“…During the long-term evolution of Opisthopappus , the dramatic geological changes and significant topographical barriers of Taihang Mountains could limit the large-scale population expansion and gradually introduce heterogeneity within different populations of O. taihangensis and O. longilobus [ 28 ]. O. taihangensis and O. longilobus were likely diverged during the early Miocene under a strengthening East Asian monsoon [ 29 ]. Subsequently, the dramatic climatic transformation and complex topography of the Taihang Mountains further promoted differentiations between the two species and their populations [ 29 ].…”

“…O. taihangensis and O. longilobus were likely diverged during the early Miocene under a strengthening East Asian monsoon [ 29 ]. Subsequently, the dramatic climatic transformation and complex topography of the Taihang Mountains further promoted differentiations between the two species and their populations [ 29 ]. At the present, O. taihangensis and O. longilobus occupy different niches due to difference in growth habits [ 30 ].…”

“…At the present, O. taihangensis and O. longilobus occupy different niches due to difference in growth habits [ 30 ]. According to the current geographical distribution of O. taihangensis and O. longilobus , we presumed that adaptive divergence processes might have played an additional role in maintaining the differentiation of the two Opisthopappus species that inhabit different regions of the Taihang Mountains [ 29 ]. Whether driven by morphological, genetic, or metabolic aspects, differentiation proceeded between O. taihangensis and O. longilobus .Previous genetic and phylogeographic studies on nuclear DNA, plastid DNA and transcriptome data have shown significant variation between the two species [ 28 , 30 – 34 ].…”

Analysis of terpenoids and their gene regulatory networks on the basis of the transcriptome and metabolome of Opisthopappus longilobus

“…The whole O. longilobus plant is fragrant because of the substantial abundance of aromatic oil. Moreover, from June to September (i.e., the flowering period), it produces white flowers ( Guo et al., 2013 ; Wang, 2013 ; Jia and Wang, 2015 ; Ye et al., 2021 ). Many recent studies on O. taihangensis and O. longilobus focused on genetic diversity and genetic structure, tissue culture, community characteristics, and antioxidant and antibacterial compounds ( Guo et al., 2013 ; Chai et al., 2018 ; Zhang et al., 2018 ; Ye et al., 2021 ).…”