Most cited article - PubMed ID 38868992
Ploidy as a leaky reproductive barrier: mechanisms, rates and evolutionary significance of interploidy gene flow
Understanding the relationship between macro- and microevolutionary processes and their delimitation remains a challenge. This review focuses on the role of chromosomal rearrangements in plant population differentiation and lineage diversification resulting in speciation, helping bridge the gap between macro- and microevolution through chromosomal evolution. We focus on angiosperms, a group that comprises the majority of extant plant species diversity and exhibits the largest chromosomal and genomic variations. Here, we address the following questions: Are macroevolutionary patterns of chromosome evolution the result of accumulated microevolutionary changes, or do chromosomal dynamics drive larger shifts along the speciation continuum? At the macroevolutionary level, we investigated the association between karyotype diversity and diversification rates using evidence from comparative genomics, chromosomal evolution modelling across phylogenies, and the association with several traits across different angiosperm lineages. At the microevolutionary level, we explore if different karyotypes are linked to morphological changes and population genetic differentiation in the same lineages. Polyploidy (autopolyploidy and allopolyploidy) and dysploidy are known drivers of speciation, with karyotypic differences often leading to reproductive barriers. We found that dysploidy, involving gains and losses of single chromosomes with no significant change in overall content of the genome, appears to be relatively more frequent and persistent across macroevolutionary histories than polyploidy. Additionally, chromosomal rearrangements that do not entail change in chromosome number, such as insertions, deletions, inversions, and duplications of chromosome fragments, as well as translocations between chromosomes, are increasingly recognized for their role in local adaptation and speciation. We argue that there is more evidence linking chromosomal rearrangements with genetic and morphological trait differentiation at microevolutionary scales than at macroevolutionary ones. Our findings highlight the importance of selection across evolutionary scales, where certain chromosomal dynamics become fixed over macroevolutionary time. Consequently, at microevolutionary scales, chromosome rearrangements are frequent and diverse, serving as key drivers of plant diversification and adaptation by providing a pool of variation from which beneficial chromosomal changes can be selected and fixed by evolutionary forces.
- Keywords
- angiosperms, chromosome, dysploidy, evolution, polyploidy, speciation,
- Publication type
- Journal Article MeSH
- Review MeSH
Genetic variation underpins evolutionary change, but mutation accumulation increases genetic load. Various factors affect the extent of load, such as population size and breeding system, but other important determinants remain unexplored. In particular, whole-genome duplication (WGD)-a pervasive macromutation occurring broadly across Eukaryotes-remains poorly understood in terms of its impact on neutral and selective processes within populations. Using iterative forward simulations and empirical analysis of 632 short- and 16 long-read sequenced individuals of Arabidopsis arenosa (in 23 diploid and 42 natural autotetraploid populations), we measure the effects of WGD on genome-wide diversity and mutation load. Our simulations show how genetic variation gradually rises in autotetraploids due to increased mutational target size. Moreover, mutation load increases due to relaxed purifying selection as ploidies rise, when deleterious mutations are masked by additional chromosome copies. Empirical data confirm these patterns, showing significant increases in nucleotide diversity, ratios of nonsynonymous to synonymous SNPs, and numbers of indels and large structural variants in A. arenosa autotetraploids. However, a rather modest increase in load proxies together with a broad distribution and niche of autotetraploids suggests load accumulation has not yet limited their successful expansion. Overall, we demonstrate a complex interplay between neutral processes and purifying selection in shaping genetic variation following WGD and highlight ploidy as an important determinant of mutation load, genetic diversity, and therefore adaptive potential in natural populations.
- Keywords
- Arabidopsis, evolution, genetic load, genomics, natural selection,
- MeSH
- Mutation Accumulation * MeSH
- Arabidopsis * genetics MeSH
- Gene Duplication MeSH
- Genetic Load * MeSH
- Genome, Plant * MeSH
- Polymorphism, Single Nucleotide MeSH
- Evolution, Molecular MeSH
- INDEL Mutation MeSH
- Selection, Genetic MeSH
- Genomic Structural Variation MeSH
- Tetraploidy * MeSH
- Publication type
- Journal Article MeSH
Polyploidisation is a significant reproductive barrier, yet genetic evidence indicates that interploidy admixture is more common than previously thought. Theoretical models and controlled crosses support the 'triploid bridge' hypothesis, proposing that hybrids of intermediate ploidy facilitate gene flow. However, comprehensive evidence combining experimental and genetic data from natural mixed-ploidy species is missing. Here, we investigated the rates and directionality of gene flow within a diploid-autotetraploid contact zone of Cardamine amara, a species with abundant natural triploids. We cytotyped over 400 individuals in the field, conducted reciprocal interploidy crosses, and inferred gene flow based on genome-wide sequencing of 84 individuals. Triploids represent a conspicuous entity in mixed-ploidy populations (5%), yet only part of them arose through interploidy hybridisation. Despite being rarely formed, triploid hybrids can backcross with their parental cytotypes, producing viable offspring that are often euploid (in 42% of cases). In correspondence, D-statistics and coalescent simulations documented a significant genome-wide signal of bidirectional gene flow in sympatric but not allopatric populations. Triploids, though rare, thus seem to play a key role in overcoming polyploidy-related reproductive barriers in C. amara. In sum, we present integrative evidence for interploidy gene flow mediated by a triploid bridge in natural populations.
- Keywords
- introgression, polyploidy, population genomics, speciation, whole genome duplication,
- MeSH
- Cardamine * genetics MeSH
- Genetic Introgression * MeSH
- Hybridization, Genetic MeSH
- Ploidies * MeSH
- Polyploidy MeSH
- Genetics, Population MeSH
- Gene Flow * MeSH
- Triploidy * MeSH
- Publication type
- Journal Article MeSH