Ploidy as a leaky reproductive barrier: mechanisms, rates and evolutionary significance of interploidy gene flow

Abstract

Background: Whole-genome duplication (polyploidization) is a dominant force in sympatric speciation, particularly in plants. Genome doubling instantly poses a barrier to gene flow owing to the strong crossing incompatibilities between individuals differing in ploidy. The strength of the barrier, however, varies from species to species and recent genetic investigations revealed cases of rampant interploidy introgression in multiple ploidy-variable species.

Scope: Here, we review novel insights into the frequency of interploidy gene flow in natural systems and summarize the underlying mechanisms promoting interploidy gene flow. Field surveys, occasionally complemented by crossing experiments, suggest frequent opportunities for interploidy gene flow, particularly in the direction from diploid to tetraploid, and between (higher) polyploids. However, a scarcity of accompanying population genetic evidence and a virtual lack of integration of these approaches leave the underlying mechanisms and levels of realized interploidy gene flow in nature largely unknown. Finally, we discuss potential consequences of interploidy genome permeability on polyploid speciation and adaptation and highlight novel avenues that have just recently been opened by the very first genomic studies of ploidy-variable species. Standing in stark contrast with rapidly accumulating evidence for evolutionary importance of homoploid introgression, similar cases in ploidy-variable systems are yet to be documented.

Conclusions: The genomics era provides novel opportunity to re-evaluate the role of interploidy introgression in speciation and adaptation. To achieve this goal, interdisciplinary studies bordering ecology and population genetics and genomics are needed.

Keywords: Adaptation; evolution; genetic introgression; polyploidy; speciation; whole-genome duplication.

Fig. 1.

Three non-exclusive scenarios for interploidy admixture, exemplified on a diploid (2x)–tetraploid (4x) system. (A) Unidirectional gene flow mediated by unreduced gametes of the lower-ploidy cytotype (2x). (B) Bidirectional interploidy gene flow mediated by (partially) fertile individuals of intermediate ploidy (triploids, 3x, in this example). (C) Recurrent origins of polyploids followed by homoploid hybridization upon secondary contact of tetraploids, enabling admixture of different ancestral diploid pools in tetraploid individuals. Thick black linse represent the reproductive isolation barrier (e.g. prezygotic, spatial or postzygotic in the case of progressed diploid speciation). The rectangles denote individuals and circles represent gametes with a reduced or unreduced number of chromosomes. Note that under (A) and possibly also (C), fertile triploid formation is not a precondition for interploidy gene flow, implying that genetic isolation may be imperfect even in cases of strong reproductive barriers; in such cases, however, interploidy gene flow can only occur unidirectionally from diploid to tetraploid.

Fig. 2.

Examples of mixed-ploidy plant systems with documented presence of fertile interploidy hybrids and significant interploidy gene flow. (A) Arabidopsis arenosa (Brassicaceae), (B) Alnus glutinosa species group (Betulaceae), (C) Senecio carniolicus species group (Asteraceae), and (D) Tripleurospermum inodorum (Asteraceae). (Photographs: F. Kolář).

Fig. 3.

Topologies of gene and species trees under different scenarios of diploid–tetraploid relationships between sympatric (S) diploid and tetraploid populations and an additional allopatric (A) tetraploid population. (A) Sketch of the spatial arrangement of the sampled populations and gene trees supporting multiple tetraploid origins (or post-WGD interploidy gene flow; solid lines) or single tetraploid origin (or post-WGD homoploid gene flow; dashed lines). (B) Single polyploid origin without gene flow, involving only incomplete lineage sorting (ILS). (C) Recurrent polyploidization and subsequent homoploid gene flow between the tetraploid lineages (corresponds with the mechanism in Fig. 1C). (D) Single polyploid origin, ILS and unidirectional interploidy gene flow in the direction 2x → 4x in the zone of sympatry (S; corresponds with the mechanisms in Fig. 1A and partially also Fig. 1B).