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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.
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Monoicy, dioicy, and genetic structure in three species of Sheathia (Batrachospermales, Rhodophyta)
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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- Award ID(s):
- 2436117
- PAR ID:
- 10593266
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Journal of Phycology
- ISSN:
- 0022-3646
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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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.more » « less
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Mank, Judith (Ed.)Abstract Many animal species are haplodiploid: their fertilized eggs develop into diploid females and their unfertilized eggs develop into haploid males. The unique genetic features of haplodiploidy raise the prospect that these systems can be used to disentangle the population genetic consequences of haploid and diploid selection. To this end, sex-specific reproductive genes are of particular interest because, while they are shared within the same genome, they consistently experience selection in different ploidal environments. However, other features of these genes, including sex-specific expression and putative involvement in postcopulatory sexual selection, are potentially confounding factors because they may also impact the efficacy of selection asymmetrically between the sexes. Thus, to properly interpret evolutionary genomic patterns, it is necessary to generate a null expectation for the relative amount of polymorphism and divergence we expect to observe among sex-specific genes in haplodiploid species, given differences in ploidal environment, sex-limited expression, and their potential role in sexual selection. Here, we derive the theoretical expectation for the rate of evolution of sex-specific genes in haplodiploid species, under the assumption that they experience the same selective environment as genes expressed in both sexes. We find that the null expectation is that reproductive genes evolve more rapidly than constitutively expressed genes in haplodiploid genomes. However, despite the aforementioned differences, the null expectation does not differ between male- and female-specific reproductive genes, when assuming additivity. Our theoretical results provide an important baseline expectation that should be used in molecular evolution studies comparing rates of evolution among classes of genes in haplodiploid species.more » « less
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