The global distribution of angiosperm genome size is shaped by climate

Abstract

Summary Angiosperms, which inhabit diverse environments across all continents, exhibit significant variation in genome sizes, making them an excellent model system for examining hypotheses about the global distribution of genome size. These include the previously proposed large genome constraint, mutational hazard, polyploidy‐mediated, and climate‐mediated hypotheses. We compiled the largest genome size dataset to date, encompassing 16 017 (> 5% of known) angiosperm species, and analyzed genome size distribution using a comprehensive geographic distribution dataset for all angiosperms. We observed that angiosperms with large range sizes generally had small genomes, supporting the large genome constraint hypothesis. Climate was shown to exert a strong influence on genome size distribution along the global latitudinal gradient, while the frequency of polyploidy and the type of growth form had negligible effects. In contrast to the unimodal patterns along the global latitudinal gradient shown by plant size traits and polyploid proportions, the increase in angiosperm genome size from the equator to 40–50°N/S is probably mediated by different (mostly climatic) mechanisms than the decrease in genome sizes observed from 40 to 50°N northward. Our analysis suggests that the global distribution of genome sizes in angiosperms is mainly shaped by climatically mediated purifying selection, genetic drift, relaxed selection, and environmental filtering.

Environmental impacts on intraspecific variation in Ambrosia artemisiifolia genome size in Slovakia, Central Europe

“…Latitude is the most evident factor that correlates with the genome size of many plant species. In the northern hemisphere, the genome size increases from the equator to the temperate zone and decreases again towards the pole (Yu et al 2018 ; Bureš et al 2024 ). Monoploid genome size in Ambrosia species increases from subtropical regions to the temperate zone (Sliwinska et al 2009 ; Zonneveld 2019 ), but in temperate Ambrosia artemisiifolia , it is again smaller (Kubešová et al 2010 ; Pustahija et al 2013 ; Zonneveld 2019 ).…”

“…In contrast, the intraspecific variation among populations or individuals was revealed for a small number of species (e.g., Festuca pallens , Šmarda and Bureš 2006 ; Šmarda et al 2008 , 2010 , Lythrum salicaria , Kubátová et al 2008 ; Phragmites australis , Meyerson et al 2016 ; Pyšek et al 2020 , or Euphrasia arctica , Becher et al 2021 ). The plant genome size can be linked for various species or taxonomic groups with life cycle and life form (Bennett 1972 ; Albach and Greilhuber 2004 ; Hidalgo et al 2015 ; Shao et al 2021 ; Carta et al 2022 ), growth form (Ohri 2005 ; Dušková et al 2010 ; Trávníček et al 2019 ), climatic factors (Bennett et al 1982 ; Bennett 1987 ; Wakamiya et al 1993 ; Caceres et al 1998 ; Carta and Peruzzi 2016 ), geographical features (Levin and Funderburg 1979 ; Rayburn 1990 ; Bottini et al 2000 ; Knight et al 2005 ; Meyerson et al 2016 ; Bureš et al 2024 ), invasiveness (Bennett et al 1998 ; Grotkopp et al 2004 ; Kubešová et al 2010 ; Pyšek et al 2020 ), stress factors or pollution (Madlung and Comai 2004 ; Vidic et al 2009 ; Meyerson et al 2020 ), metabolic resources such as phosphorus and nitrogen (Hessen et al 2010 ; Guignard et al 2016 ), or phylogenetic age (Farah et al 2018 ; Hoang et al 2020 ). Despite much evidence of adaptive selection, genetic drift cannot be excluded from the genome size distribution (Blommaert 2020 ).…”

“…Some intraspecific variation in ragweed genome size is documented as its DNA amount varies from 2.08 to 2.27 pg/2C (Kubešová et al 2010 ; Bai et al 2012 ; Battlay et al 2023 ). However, this variability has not been linked to environmental factors that are known to affect genome size selection (Knight and Ackerly 2002 ; Knight et al 2005 ; Bureš et al 2024 ).…”

Morphological and habitat differentiation between diploids and tetraploids of a Drakensberg near‐endemic taxon, Rhodohypoxis baurii var. platypetala (Hypoxidaceae)

“…Polyploidy, where organisms possess more than two complete sets of chromosomes in the nuclei (de Wet, 1971;Otto & Whitton, 2000;Ramsey & Schemske, 1998), is widely considered an important mechanism of evolution in angiosperms (Ramsey & Ramsey, 2014;Weiss-Schneeweiss et al, 2013;Wood et al, 2009). Polyploid plants are globally distributed, and environmental factors such as annual mean temperature and latitude have been suggested as key drivers of this global distribution (Bureš et al, 2024;Rice et al, 2019). These variables are likely influencing range boundaries of different ploidy levels.…”

Reductional dysploidy and genome size diversity in Pooideae, the largest subfamily of grasses (Poaceae)

“…groups of closely individual species or microtaxa/microspecies differing by their ploidy levels, such differences in distribution or ecological behavior have long been known and are among the classic examples of 'cytogeography'. DNA quanti cation, especially by ow cytometry, which is well established as a reliable and accurate method, provides a time-saving and e cient way to study such differentiation processes at different scales, from variation within populations to large areas of distribution (Paule et Bureš et al 2024). In addition to the saltational changes caused by polyploidization, gradual, more or less continuous changes in genome size can also be detected, sometimes even between populations or closely related taxa, which typically result primarily from the ampli cation of mobile elements in the genome and their gradual loss over longer periods of time, leading to genome enlargement or reduction (Zedek et Many genera of Pooideae show a strong proliferation of annual species, a well-known process of angiosperm life form evolution (Hjertaas et al 2023) that is often associated with changes in genome size (Bennett and Leitch 2005; Knight et al 2005; Leitch and Bennett 2007).…”