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Abstract Sexual systems (i.e., separate vs. combined sexes) vary widely among eukaryotes and influence the evolution of reproductive systems, which shape genetic structure and evolutionary trajectories. In diploid‐dominant angiosperms, combined (i.e., hermaphroditism) and separate sexes are expected to correlate with selfing and outcrossing, respectively. When sex is determined in the haploid phase, selfing is possible even when there are separate sexes. The freshwater red macroalgal genusSheathia(Batrachospermales) displays sexual system variation within and among populations, but no prior data exist on the reproductive systems of these populations. We developed 16 polymorphic microsatellite loci to characterize the reproductive system and genetic structure of threeSheathiaspecies. We observed cross‐amplification of loci across the three targeted species, suggesting these markers may be useful in otherSheathiaspp. We observed variation in monoicy (i.e., hermaphroditism) versus dioicy (i.e., separate sexes) in each species, includingS. americana, which was previously believed to be obligately dioicous. Our data suggest thatS. americanaandS. involutadisplay more variation in their prevailing reproductive modes as compared toS. grandis. Generally, dioicy resulted in greater diversity in contrast to monoicy. We observed strong population structure that is likely driven by uniparental reproduction and limited dispersal; however, there is limited population connectivity that may be facilitated by long‐distance dispersal events. Overall, these data contribute to our knowledge of the relationship between the sexual system, reproductive system, and population genetic structure in haploid‐diploid taxa, thereby informing a broader understanding of the evolution of sex.
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Seasonality and interannual stability in the population genetic structure of Batrachospermum gelatinosum (Rhodophyta)
Abstract Temporal population genetic studies have investigated evolutionary processes, but few have characterized reproductive system variation. Yet, temporal sampling may improve our understanding of reproductive system evolution through the assessment of the relative rates of selfing, outcrossing, and clonality. In this study, we focused on the monoicous, haploid‐diploid freshwater red algaBatrachospermum gelatinosum. This species has a perennial, microscopic diploid phase (chantransia) that produces an ephemeral, macroscopic haploid phase (gametophyte). Recent work focusing on single‐time point genotyping suggested high rates of intragametophytic selfing, although there was variation among sites. We expand on this work by genotyping 191 gametophytes sampled from four sites that had reproductive system variation based on single‐snapshot genotyping. For this study, we sampled at multiple time points within and among years. Results from intra‐annual data suggested shifts in gametophytic genotypes throughout the season. We hypothesize that this pattern is likely due to the seasonality of the life cycle and the timing of meiosis among the chantransia. Interannual patterns were characterized by consistent genotypic and genetic composition, indicating stability in the prevailing reproductive system through time. Yet, our study identified limits by which available theoretical predictions and analytical tools can resolve reproductive system variation using haploid data. There is a need to develop new analytical tools to understand the evolution of sex by expanding our ability to characterize the spatiotemporal variation in reproductive systems across diverse life cycles.
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- Award ID(s):
- 2436117
- PAR ID:
- 10621598
- Publisher / Repository:
- wiley
- Date Published:
- Journal Name:
- Journal of Phycology
- Volume:
- 61
- Issue:
- 1
- ISSN:
- 0022-3646
- Page Range / eLocation ID:
- 172 to 193
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract The relative frequency of sexual versus asexual reproduction governs the distribution of genetic diversity within and among populations. Most studies on the consequences of reproductive variation focus on the mating system (i.e., selfing vs. outcrossing) of diploid‐dominant taxa (e.g., angiosperms), often ignoring asexual reproduction. Although reproductive systems are hypothesized to be correlated with life‐cycle types, variation in the relative rates of sexual and asexual reproduction remains poorly characterized across eukaryotes. This is particularly true among the three major lineages of macroalgae (green, brown, and red). The Rhodophyta are particularly interesting, as many taxa have complex haploid–diploid life cycles that influence genetic structure. Though most marine reds have separate sexes, we show that freshwater red macroalgae exhibit patterns of switching between monoicy and dioicy in sister taxa that rival those recently shown in brown macroalgae and in angiosperms. We advocate for the investigation of reproductive system evolution using freshwater reds, as this will expand the life‐cycle types for which these data exist, enabling comparative analyses broadly across eukaryotes. Unlike their marine cousins, species in the Batrachospermales have macroscopic gametophytes attached to filamentous, often microscopic sporophytes. While asexual reproduction through monospores may occur in all freshwater reds, the Compsopogonales are thought to be exclusively asexual. Understanding the evolutionary consequences of selfing and asexual reproduction will aid in our understanding of the evolutionary ecology of all algae and of eukaryotic evolution generally.more » « less
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Variation in selfing rates within and among populations of hermaphroditic flowering plants can strongly influence the evolution of reproductive strategies and the genetic structure of populations. This intraspecific variation in mating patterns may reflect both genetic and ecological factors, but the relative importance of these factors remains poorly understood. Here, we explore how selfing in 13 natural populations of the perennial wildflower Mimulus ringens is influenced by (a) pollinator visitation, an ecological factor, and (b) floral display, a trait with a genetic component that also responds to environmental variation. We also explore whether genetically based floral traits, including herkogamy, affect selfing. We found substantial variation among populations in selfing rate (0.13–0.55). Selfing increased strongly and significantly with floral display, among as well as within populations. Selfing also increased at sites with lower pollinator visitation and low plant density. However, selfing was not correlated with floral morphology. Overall, these results suggest that pollinator visitation and floral display, two factors that interact to affect geitonogamous pollinator movements, can influence the selfing rate. This study identifies mechanisms that may play a role in maintaining selfing rate variation among populations.more » « less
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Abstract The freshwater red algaBatrachospermum gelatinosumhas a well‐documented distribution spanning historically glaciated and unglaciated eastern North America. This alga has no known desiccation‐resistant propagule; thus, long‐distance dispersal events are likely rare. We predicted strong genetic structure among drainage basins and admixture among sites within basins. We predicted greater genetic diversity at lower latitude sites because they likely serve as refugia and the origin of northward, post‐Pleistocene range expansion. We used 10 microsatellite loci to investigate genetic diversity from 311 gametophytes from 18 sites in five major drainage basins: South Atlantic Gulf, Mid‐Atlantic, Ohio River, Great Lakes, and Northeast. Our data showed strong genetic partitioning among drainage basins and among sites within basins, yet no isolation by distance was detected. Genetic diversity varied widely among sites and was not strictly related to latitude as predicted. The results fromB. gelatinosumprovide strong support that each stream site contributes to the unique genetic variation within the species, potentially due to limited dispersal and the prevailing reproductive mode of intragametophytic selfing. Simulations of migration suggested post‐Pleistocene dispersal from the Mid‐Atlantic.Batrachospermum gelatinosumpotentially persisted in refugia that were just south of the ice margins rather than in the southernmost part of its range. Research of other taxa with similar ranges could determine whether these results are generally applicable for freshwater red algae. Nevertheless, these results fromB. gelatinosumadd to the growing literature focused on the patterns and genetic consequences of post‐Pleistocene range expansion by eastern North American biota.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1111/jpy.13539
