Gene duplications and phylogenomic conflict underlie major pulses of phenotypic evolution in gymnosperms

Abstract

Inferring the intrinsic and extrinsic drivers of species diversification and phenotypic disparity across the Tree of Life is a major challenge in evolutionary biology. In green plants, polyploidy (or whole-genome duplication, WGD) is known to play a major role in microevolution and speciation, but the extent to which WGD has shaped macroevolutionary patterns of diversification and phenotypic innovation across plant phylogeny remains an open question. Here we examine the relationship of various facets of genomic evolution (including gene and genome duplication, genome size, and chromosome number) with macroevolutionary patterns of phenotypic innovation, species diversification, and climatic occupancy in gymnosperms. We show that genomic changes, including WGD, underlie the origins of most major gymnosperm clades, and that spikes of gene duplication typically coincide with major spikes of phenotypic innovation. Increased rates of phenotypic evolution, however, are typically found at nodes with high gene-tree conflict, representing historic population-level dynamics during speciation. Most shifts in gymnosperm diversification since the rise of angiosperms are decoupled from putative WGDs and instead are associated with increased rates of climatic occupancy evolution, particularly in cooler and/or more arid climatic conditions, suggesting that ecological opportunity, especially in the latter Cenozoic, and environmental heterogeneity have driven a resurgence of gymnosperm diversification. Our study provides critical insight on the processes underlying diversification and phenotypic evolution in gymnosperms, with important broader implications for the major drivers of both micro- and macroevolution in plants.

Early diversifications of angiosperms and their insect pollinators: were they unlinked?

“…The lack of increased family-level diversity of the Cretaceous entomofauna is better understood in the context of mid-Cretaceous 'turnover'. This refers to the transformation of insect communities caused by the replacement of gymnosperms by angiosperms as the increasingly dominant component of the landscape [39,[47][48][49][50]. Lineages that were closely associated with insect-pollinated gymnosperms, such as Mesopsycidae (scorpionflies) or Zhangsolvidae (flies), went extinct [50].…”

“…The harsh climates now occupied by conifers, which form the largest proportion of acrogymnosperm diversity, might have driven the move towards wind pollination of extant gymnosperms. This is especially pertinent given that many extant groups of cycads and conifers emerged in the Cenozoic, and are not evolutionary remnants of their Mesozoic ancestors [49,56,57].…”

Origin and evolution of green plants in the light of key evolutionary events

“… The widespread whole genome duplications (WGDs) and putative horizontal gene transfers (HGTs) in green plants The green plant phylogeny is based on One Thousand Plant Transcriptomes Initiative (2019). The red dots represent the putative WGDs inferred by Wood et al (2009), Devos et al (2016), Ren et al (2018), One Thousand Plant Transcriptomes Initiative (2019), Gao et al (2020), Huang et al (2020), Silva et al (2021) and Stull et al (2021). The putative HGT events and their potential functions of HGT‐derived genes in green plants are shown.…”

“…Whole-genome duplication, or polyploidy, has long been recognized as a ubiquitous phenomenon during land plant evolution. Numerous studies have implicated that recent and ancient polyploidization events occurred repeatedly throughout all the major land plant lineages, with the most frequency of WGD in angiosperms (Figure 4; Jiao et al, 2011Jiao et al, , 2014Li et al, 2015c;Ren et al, 2018;One Thousand Plant Transcriptomes Initiative, 2019;Huang et al, 2020;Wu et al, 2020;Zhang et al, 2020c;Stull et al, 2021). Ancient polyploidy in the ancestry of angiosperms and seed plants has been identified (Jiao et al, 2011), and over 180 WGDs have been further reported in all extant angiosperm lineages (One Thousand Plant Transcriptomes Initiative, 2019).…”

Polyploid clades tend to be more speciose than their putative sister clades

“…Prior studies have stressed the link between polyploidy and speciation in angiosperms 71 , with most major angiosperm clades inferred to have polyploid ancestry 72 . While genomic changes such as WGDs have been found to correlate with the origins of major gymnosperm clades as well as the root of gymnosperms itself, more recent shifts in gymnosperm diversi cation seem to be decoupled from putative WGDs 73 . We were able to identify few documented instances of natural polyploids in basal angiosperms and gymnosperms, either because polyploidy is genuinely rare 74 , or because any gene duplications were su ciently ancient to obfuscate its signal 21 .…”