Drivers of diversification in Linum (Linaceae) by means of chromosome evolution: correlations with biogeography, breeding system and habit

Abstract

Background and aims: Chromosome evolution leads to hybrid dysfunction and recombination patterns and has thus been proposed as a major driver of diversification in all branches of the tree of life, including flowering plants. In this study we used the genus Linum (flax species) to evaluate the effects of chromosomal evolution on diversification rates and on traits that are important for sexual reproduction. Linum is a useful study group because it has considerable reproductive polymorphism (heterostyly) and chromosomal variation (n = 6-36) and a complex pattern of biogeographical distribution.

Methods: We tested several traditional hypotheses of chromosomal evolution. We analysed changes in chromosome number across the phylogenetic tree (ChromEvol model) in combination with diversification rates (ChromoSSE model), biogeographical distribution, heterostyly and habit (ChromePlus model).

Key results: Chromosome number evolved across the Linum phylogeny from an estimated ancestral chromosome number of n = 9. While there were few apparent incidences of cladogenesis through chromosome evolution, we inferred up to five chromosomal speciation events. Chromosome evolution was not related to heterostyly but did show significant relationships with habit and geographical range. Polyploidy was negatively correlated with perennial habit, as expected from the relative commonness of perennial woodiness and absence of perennial clonality in the genus. The colonization of new areas was linked to genome rearrangements (polyploidy and dysploidy), which could be associated with speciation events during the colonization process.

Conclusions: Chromosome evolution is a key trait in some clades of the Linum phylogeny. Chromosome evolution directly impacts speciation and indirectly influences biogeographical processes and important plant traits.

Keywords: Breeding system; Linaceae; diversification; dysploidy; flax; heterostyly; polyploidy.

Fig. 1.

Chromosome number reconstruction based on the ChromEvol ‘CONST_RATE_DEMI’ model for the dataset with the median chromosome number. Chromosome numbers and probabilities (in plot charts) are shown with different colours. Trait states for chromosome number, heterostyly, biogeography and habit are indicated at the tips of the phylogeny.

Fig. 2.

Chromosome number reconstruction based on the ChromoSSE model for the dataset with the median chromosome number. Chromosome numbers are shown with different colours and posterior probabilities with the size of the dots. Chromosomal cladogenetic events are indicated with arrows.

Fig. 3.

(A) Posterior probability densities of the estimates of the anagenetic parameters in the ChromoSSE model. The x-axis displays the rate of anagenetic parameters; the y-axis indicates the posterior probability density of each value. (B) Posterior probability densities of the estimates of the cladogenetic parameters in the ChromoSSE model. The x-axis displays the rate of cladogenetic parameters; the y-axis indicates the posterior probability density of each value.

Fig. 4.

Histograms of chromosome number for (A) heterostyly: monomorphic (yellow) vs. polymorphic (blue); (B) biogeography: source (yellow) vs. colonized (blue) areas; and (C) habit: annual (yellow) vs. perennial (blue). The x-axis indicates the chromosome number and the y-axis displays the frequency of the chromosome number for each trait.

Fig. 5.

Correlation between chromosome evolution and biogeography. Values indicate the rates of chromosomal change for Linum species in the source area (blue) and in colonized (red) areas. Rates are proportional to arrow and circle thicknesses.