Recently Formed Polyploid Plants Diversify at Lower Rates

Abstract

Polyploidy, the doubling of genomic content, is a widespread feature, especially among plants, yet its macroevolutionary impacts are contentious. Traditionally, polyploidy has been considered an evolutionary dead end, whereas recent genomic studies suggest that polyploidy has been a key driver of macroevolutionary success. We examined the consequences of polyploidy on the time scale of genera across a diverse set of vascular plants, encompassing hundreds of inferred polyploidization events. Likelihood-based analyses indicate that polyploids generally exhibit lower speciation rates and higher extinction rates than diploids, providing the first quantitative corroboration of the dead-end hypothesis. The increased speciation rates of diploids can, in part, be ascribed to their capacity to speciate via polyploidy. Only particularly fit lineages of polyploids may persist to enjoy longer-term evolutionary success.

Polyploid Evolution of the Brassicaceae during the Cenozoic Era

“…Polyploidy has both costs and benefits, and under stable environmental conditions, polyploidy is considered to be disadvantageous due to the reduced fitness of polyploid individuals caused by their reproductive isolation and lower fertility (Comai, 2005). The lower speciation/diversification rates and higher extinction rates observed in neopolyploids compared with diploids (Mayrose et al, 2011) could be due to sampling errors and methodological shortcomings (Soltis et al, 2014) or may also be a consequence of the outweighing costs of polyploidy associated genomic and phenotypic instability, as well as the reproductive disadvantages under normal conditions. However, the adaptive advantages of polyploidy caused by enhanced genetic repertoire (resulting from increased heterozygosity, the buffering effect of gene redundancy on mutations, neofunctionalization, differential expression, or epigenetic reprogramming of duplicated genes) and reproductive plasticity (facilitation of reproduction through selffertilization or asexual means) would be expected to confer a competitive advantage to polyploid species under extreme and unstable environmental conditions (Comai, 2005;Fawcett and Van de Peer, 2010).…”

Can resource costs of polyploidy provide an advantage to sex?

“…The idea that ploidy affects organismal ecology has a long history (Vandel, 1928;Stebbins, 1938;Suomalainen, 1950;Cavalier-Smith, 1978;Bell, 1982;Levin, 1983;Bierzychudek, 1985), but there is still no consensus on whether there are definitive advantages or costs of polyploidy that can explain its frequency and distribution (Mable and Otto, 1998;Mable, 2001;Ramsey and Schemske, 2002;Zeyl, 2004;Buggs and Pannell, 2007;Gerstein and Otto, 2009;Soltis et al, 2010;Beck et al, 2011;Mayrose et al, 2011;Ramsey, 2011). The advantages and disadvantages of polyploidy and its relevance to the distribution and maintenance of sex have been reviewed extensively (Bierzychudek, 1985 The ecological consequences of polyploidy are difficult to empirically disentangle from those directly related to asexuality, with which it is so often associated (Bierzychudek, 1985;Otto and Whitton, 2000;Hörandl, 2006;Mable et al, 2011).…”

Polyploidy and novelty: Gottlieb's legacy

“…Thus, not only does polyploidization yield a single new species, but also gene and genome dynamics following polyploid formation are predicted, in many cases, to trigger a species radiation [133], such as those observed at deep phylogenetic levels in yeast [17,134], teleost fishes [135,136] and angiosperms (e.g. [137][138][139], but see [140]). The impacts of genetic and phenotypic novelty in shaping variable polyploid populations are thus amplified through accelerated formation of reproductive barriers between genetically divergent individuals, leading to greater diversity than generated through the original polyploidization event.…”