Phylogenomic insights into the origin and evolutionary history of evergreen broadleaved forests in East Asia under Cenozoic climate change

Abstract

The evergreen versus deciduous leaf habit is an important functional trait for adaptation of forest trees and has been hypothesized to be related to the evolutionary processes of the component species under paleoclimatic change, and potentially reflected in the dynamic history of evergreen broadleaved forests (EBLFs) in East Asia. However, knowledge about the shift of evergreen versus deciduous leaf with the impact of paleoclimatic change using genomic data remains rare. Here, we focus on the Litsea complex (Lauraceae), a key lineage with dominant species of EBLFs, to gain insights into how evergreen versus deciduous trait shifted, providing insights into the origin and historical dynamics of EBLFs in East Asia under Cenozoic climate change. We reconstructed a robust phylogeny of the Litsea complex using genome‐wide single‐nucleotide variants (SNVs) with eight clades resolved. Fossil‐calibrated analyses, diversification rate shifts, ancestral habit, ecological niche modelling and climate niche reconstruction were employed to estimate its origin and diversification pattern. Taking into account studies on other plant lineages dominating EBLFs of East Asia, it was revealed that the prototype of EBLFs in East Asia probably emerged in the Early Eocene (55–50 million years ago [Ma]), facilitated by the greenhouse warming. As a response to the cooling and drying climate in the Middle to Late Eocene (48–38 Ma), deciduous habits were evolved in the dominant lineages of the EBLFs in East Asia. Up to the Early Miocene (23 Ma), the prevailing of East Asian monsoon increased the extreme seasonal precipitation and accelerated the emergence of evergreen habits of the dominant lineages, and ultimately shaped the vegetation resembling that of today.

Meta‐analysis provides insights into the origin and evolution of East Asian evergreen broad‐leaved forests

“…Previous studies have estimated the stem ages of some clades in the Oligocene and even the Eocene, whereas their crown ages were at the Oligocene–Miocene boundary or younger ( Davidia , Ma et al ., 2015; Cyclocarya , Kou et al ., 2016; Lindera sect. Daphnidium , Qin et al ., 2023). Considering the ecological and evolutionary significance of crown and stem ages, treating these stem ages as evidence of the Oligocene or Eocene origin of the EAEBLFs may be misleading.…”

“…Subsequently, a rapid diversification event has occurred during the late Miocene (10–8 Ma, Deng et al ., 2018; Chen et al ., 2020). By contrast, other studies proposed an earlier origin of the EAEBLFs (probably during the Eocene, Heptapleurum , Li & Wen, 2014; Tetrastigma , Peng et al ., 2021; Neolitsea , Qin et al ., 2023; Ilex , Yao et al ., 2021). Thus, studies using molecular dating of different lineages have not reached a consensus on the time of EAEBLF origin.…”

The Origin of Evergreen Broad-Leaved Forests in East Asia from the Evidence of Floristic Elements

“…A key lineage in the subtropical evergreen broad-leaved forest in East Asia, Litsea complex (Lauraceae), was phylogenomically analyzed, combining the geological and paleontological records and the Cenozoic climate change [ 74 ]. It was revealed that the prevailing of the East Asian monsoon system in the Early Miocene accelerated the evolution of evergreen habits and ultimately contributed to the modernization of the subtropical evergreen broad-leaved forest in East Asia [ 74 ]. Although we approve of this suggestion, the palaeobotanical evidence reveals that southwestern and southeastern China had different vegetation in the Miocene.…”

Anthropogenic disturbance driving population decline of a dominant tree in East Asia evergreen broadleaved forests over the last 11,000 years

“…This extent covered subtropical East Asia and represented the entire natural geographic range of L. elongata (Figure 2c; Appendix S14). We also sampled L. pseudoelongata H. Liu, L. acutivena Hayata, and L. verticillata Hance as outgroup taxa based on our previous work (Qin et al., 2023). Total genomic DNA was extracted from fresh leaves, and library preparation and sequencing on the BGISEQ‐500 were conducted by BGI Genomics.…”

“…verticillata Hance as outgroup taxa based on our previous work (Qin et al, 2023). Total genomic DNA was extracted from fresh leaves, and library preparation and sequencing on the BGISEQ-500 were conducted by BGI Genomics.…”