Why do tropical plants often have smaller genomes? Genome size evolution in Cactaceae is shaped by geographically structured polyploidy

Abstract

Genomic traits (e.g. chromosome number, polyploidy, genome size—GS) often show correlations with the geographical distribution of species. However, the underlying drivers which underpin the relationships between genomic and ecological variables, and consequently biogeographical patterns, remain elusive. We investigated the biogeographical impacts of genomic traits in the dry-climate specialized family Cactaceae. We used flow cytometry to generate original GS data for Melocactus, Discocactus, and Leuenbergeria species, which, together with additional values compiled from previous publications, resulted in data for 332 (18%) species belonging to 65 (43%) genera of Cactaceae. Interactions between genomic and ecological traits were verified by using both Pearson’s correlation coefficient and phylogenetic comparative methods. Flow cytometry histograms revealed different ploidy levels within the same individual (endoreduplication) depending on the tissue analysed. 1C-values varied 15.31-fold in Cactaceae, with the largest variations in GS and ploidy levels found in the Cactoideae II and Opuntioideae clades. We found incongruences between the nuclear and plastid topologies of Cactaceae. Remarkably, both topologies revealed similar age for the main clades, with Opuntoideae polyploid lineages older (<11 Mya) than those of Cactoideae II (<4 Mya). Furthermore, the older Opuntioideae palaeopolyploids had smaller monoploid GS (1Cx) than the more recent neopolyploids. A positive correlation was observed between 1C-values and latitude, with a tendency for species with larger genomes and higher levels of polyploidy (up to 29×) in higher latitudes. In contrast, the 1Cx vs. latitude relationship showed the opposite trend. Pearson correlation analyses between GS and ecological variables showed that nuclear DNA content was mainly associated with precipitation traits. On the other hand, phylogenetic correlations (phylogenetic independent contrasts) between genomic and ecological traits revealed low/nonsignificance for both plastid and nuclear topologies. Our data demonstrate a clear role of polyploidy followed by diploidization in underpinning the geographical distribution of cacti. We hypothesize that endoreduplication, such as in the epidermis, enables diploid species with small GS to act physiologically as a polyploid in specific tissues, masking relationships between GS and ecological traits. Thus, polyploidy (including endopolyploidy) has played a role in shaping the biogeographical history and diversification of Cactaceae lineages.