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Turnovers of sex-determining systems represent important diversifying forces across eukaryotes. Shifts in sex chromosomes—but conservation of the master sex-determining genes—characterize distantly related animal lineages. Yet in plants, in which separate sexes have evolved repeatedly and sex chromosomes are typically homomorphic, we do not know whether such translocations drive sex-chromosome turnovers within closely related taxonomic groups. This phenomenon can only be demonstrated by identifying sex-associated nucleotide sequences, still largely unknown in plants. The wild North American octoploid strawberries (Fragaria) exhibit separate sexes (dioecy) with homomorphic, female heterogametic (ZW) inheritance, yet sex maps to three different chromosomes in different taxa. To characterize these turnovers, we identified sequences unique to females and assembled their reads into contigs. For most octoploid Fragaria taxa, a short (13 kb) sequence was observed in all females and never in males, implicating it as the sex-determining region (SDR). This female-specific “SDR cassette” contains both a gene with a known role in fruit and pollen production and a novel retrogene absent on Z and autosomal chromosomes. Phylogenetic comparison of SDR cassettes revealed three clades and a history of repeated translocation. Remarkably, the translocations can be ordered temporally due to the capture of adjacent sequence with each successive move. The accumulation of the “souvenir” sequence—and the resultant expansion of the hemizygous SDR over time—could have been adaptive by locking genes into linkage with sex. Terminal inverted repeats at the insertion borders suggest a means of movement. To our knowledge, this is the first plant SDR shown to be translocated, and it suggests a new mechanism (“move-lock-grow”) for expansion and diversification of incipient sex chromosomes. [ABSTRACT FROM AUTHOR]

Disentangling the evolutionary histories of polyploids, especially those with high ploidies, can reveal fundamental processes in speciation. Despite occurring frequently during evolution, the origins of many extant polyploid plant species remain largely unknown., By integrating linkage mapping, polyploid phylogeny and sex-determining region ( SDR) in a unified framework, we statistically evaluated evolutionary hypotheses concerning the origin of a recently recognized decaploid strawberry ( Fragaria cascadensis)., The maximum-likelihood phylogenies and topology tests across homeologous groups consistently rejected the seemingly parsimonious hypothesis of 'contemporary sympatric speciation' via hybridization between octoploid and diploid congeners. Instead, most chromosomes supported 'ancient hybrid speciation' between a maternal octoploid progenitor ancestral to extant octoploid strawberries and a paternal, extinct Fragaria iinumae-like diploid progenitor, probably in Beringia during the Pleistocene. The absence of a shared SDR between the decaploid and other Fragaria is also consistent with an older origin rather than a recent hybrid origin in situ., Our study reveals a long evolutionary history of the decaploid despite its recent discovery, and highlights the pitfalls of inferring polyploid origins from niche/range alone or combined with morphology. It can serve as an exemplary starting step towards building much-needed model systems of established polyploids that have been, and remain to be, recognized. [ABSTRACT FROM AUTHOR]

With their extraordinary diversity in sexual systems, flowering plants offer unparalleled opportunities to understand sex determination and to reveal generalities in the evolution of sex chromosomes. Comparative genetic mapping of related taxa with good phylogenetic resolution can delineate the extent of sex chromosome diversity within plant groups, and lead the way to understanding the evolutionary drivers of such diversity. The North American octoploid wild strawberries provide such an opportunity. We performed linkage mapping using targeted sequence capture for the subdioecious western Fragaria virginiana ssp. platypetala and compared the location of its sexdetermining region (SDR) to those of 2 other (sub)dioecious species, the eastern subspecies, F. virginiana ssp. virginiana (whose SDR is at 0-5.5 Mb on chromosome VI of the B2 subgenome), and the sister species F. chiloensis (whose SDR is at 37 Mb on chromosome VI of the Av subgenome). Male sterility was dominant in F. virginiana ssp. platypetala and mapped to a chromosome also in homeologous group VI. Likewise, one major quantitative trait locus (QTL) for female fertility overlapped the male sterility region. However, the SDR mapped to yet another subgenome (B1), and to a different location (13 Mb), but similar to the location inferred in one population of the naturally occurring hybrid between F. chiloensis and F. virginiana (F. ×ananassa ssp. cuneifolia). Phylogenetic analysis of chromosomes across the octoploid taxa showed consistent subgenomic composition reflecting shared evolutionary history but also reinforced within-species variation in the SDR-carrying chromosome, suggesting either repeated evolution, or recent turnovers in SDR. [ABSTRACT FROM AUTHOR]

Summary: Recombination in ancient, heteromorphic sex chromosomes is typically suppressed at the sex‐determining region (SDR) and proportionally elevated in the pseudoautosomal region (PAR). However, little is known about recombination dynamics of young, homomorphic plant sex chromosomes.We examine male and female function in crosses and unrelated samples of the dioecious octoploid strawberry Fragaria chiloensis in order to map the small and recently evolved SDR controlling both traits and to examine recombination patterns on the incipient ZW chromosome.The SDR of this ZW system is located within a 280 kb window, in which the maternal recombination rate is lower than the paternal one. In contrast to the SDR, the maternal PAR recombination rate is much higher than the rates of the paternal PAR or autosomes, culminating in an elevated chromosome‐wide rate. W‐specific divergence is elevated within the SDR and a single polymorphism is observed in high species‐wide linkage disequilibrium with sex.Selection for recombination suppression within the small SDR may be weak, but fluctuating sex ratios could favor elevated recombination in the PAR to remove deleterious mutations on the W. The recombination dynamics of this nascent sex chromosome with a modestly diverged SDR may be typical of other dioecious plants. [ABSTRACT FROM AUTHOR]

Whole-genome duplications are radical evolutionary events that have driven speciation and adaptation in many taxa. Higher-order polyploids have complex histories often including interspecific hybridization and dynamic genomic changes. This chromosomal reshuffling is poorly understood for most polyploid species, despite their evolutionary and agricultural importance, due to the challenge of distinguishing homologous sequences from each other. Here, we use dense linkage maps generated with targeted sequence capture to improve the diploid strawberry (Fragaria vesca) reference genome and to disentangle the subgenomes of the wild octoploid progenitors of cultivated strawberry, Fragaria virginiana and Fragaria chiloensis. Our novel approach, POLiMAPS (Phylogenetics Of Linkage-Map-Anchored Polyploid Subgenomes), leverages sequence reads toassociate informative interhomeolog phylogeneticmarkers with linkage groups and reference genome positions. In contrast to a widely acceptedmodel, we find that one of the four subgenomes originates with the diploid cytoplasm donor F. vesca, one with the diploid Fragaria iinumae, and two with an unknownancestor close to F. iinumae. Extensive unidirectional introgression has converted F. iinumae-like subgenomes to bemore F. vesca-like, but never the reverse, due either to homoploid hybridization in the F. iinumae-like diploid ancestors or else strong selection spreading F. vesca-like sequence among subgenomes through homeologous exchange. In addition, divergence between homeologous chromosomes has been substantially augmented by interchromosomal rearrangements. Our phylogenetic approach reveals novel aspects of the complicated web of genetic exchanges that occur during polyploid evolution and suggests a path forward for unraveling other agriculturally and ecologically important polyploid genomes. [ABSTRACT FROM AUTHOR]