Evolutionary divergence of the sex-determining gene MID uncoupled from the transition to anisogamy in volvocine algae.
Ontology highlight
ABSTRACT:
SUBMITTER: Geng S
PROVIDER: S-EPMC5963870 | biostudies-literature |
REPOSITORIES: biostudies-literature
Similar Datasets
Project description:Male and female gametes differing in size-anisogamy-emerged independently from isogamous ancestors in various eukaryotic lineages, although genetic bases of this emergence are still unknown. Volvocine green algae are a model lineage for investigating the transition from isogamy to anisogamy. Here we focus on two closely related volvocine genera that bracket this transition-isogamous Yamagishiella and anisogamous Eudorina. We generated de novo nuclear genome assemblies of both sexes of Yamagishiella and Eudorina to identify the dimorphic sex-determining chromosomal region or mating-type locus (MT) from each. In contrast to the large (>1 Mb) and complex MT of oogamous Volvox, Yamagishiella and Eudorina MT are smaller (7-268 kb) and simpler with only two sex-limited genes-the minus/male-limited MID and the plus/female-limited FUS1. No prominently dimorphic gametologs were identified in either species. Thus, the first step to anisogamy in volvocine algae presumably occurred without an increase in MT size and complexity.
| S-EPMC6123790 | biostudies-literature
Project description:Although the gamete competition theory remains the dominant explanation for the evolution of anisogamy, well-known exceptions to its predictions have raised doubts about the completeness of the theory. One of these exceptions is isogamy in large or complex species of green algae. Here, we show that this exception may be explained in a manner consistent with a game-theoretic extension of the original theory: a constraint on the minimum size of a gamete may prevent the evolution of continuously stable anisogamy. We show that in the volvocine algae, both gametes of isogamous species retain an intact chloroplast, whereas the chloroplast of the microgamete in anisogamous species is invariably degenerate. The chloroplast, which functions in photosynthesis and starch storage, may be necessary to provision a gamete for an extended period when gamete encounter rates are low. The single chloroplast accounts for most of the volume of a typical gamete, and thus may constrain the minimum size of a gamete, preventing the evolution of anisogamy. A prediction from this hypothesis, that isogametes should be larger than the microgametes of similar-size species, is confirmed for the volvocine algae. Our results support the gamete competition theory.
| S-EPMC6235044 | biostudies-literature
Project description:BackgroundThroughout its nearly four-billion-year history, life has undergone evolutionary transitions in which simpler subunits have become integrated to form a more complex whole. Many of these transitions opened the door to innovations that resulted in increased biodiversity and/or organismal efficiency. The evolution of multicellularity from unicellular forms represents one such transition, one that paved the way for cellular differentiation, including differentiation of male and female gametes. A useful model for studying the evolution of multicellularity and cellular differentiation is the volvocine algae, a clade of freshwater green algae whose members range from unicellular to colonial, from undifferentiated to completely differentiated, and whose gamete types can be isogamous, anisogamous, or oogamous. To better understand how multicellularity, differentiation, and gametes evolved in this group, we used comparative genomics and fossil data to establish a geologically calibrated roadmap of when these innovations occurred.ResultsOur ancestral-state reconstructions, show that multicellularity arose independently twice in the volvocine algae. Our chronograms indicate multicellularity evolved during the Carboniferous-Triassic periods in Goniaceae + Volvocaceae, and possibly as early as the Cretaceous in Tetrabaenaceae. Using divergence time estimates we inferred when, and in what order, specific developmental changes occurred that led to differentiated multicellularity and oogamy. We find that in the volvocine algae the temporal sequence of developmental changes leading to differentiated multicellularity is much as proposed by David Kirk, and that multicellularity is correlated with the acquisition of anisogamy and oogamy. Lastly, morphological, molecular, and divergence time data suggest the possibility of cryptic species in Tetrabaenaceae.ConclusionsLarge molecular datasets and robust phylogenetic methods are bringing the evolutionary history of the volvocine algae more sharply into focus. Mounting evidence suggests that extant species in this group are the result of two independent origins of multicellularity and multiple independent origins of cell differentiation. Also, the origin of the Tetrabaenaceae-Goniaceae-Volvocaceae clade may be much older than previously thought. Finally, the possibility of cryptic species in the Tetrabaenaceae provides an exciting opportunity to study the recent divergence of lineages adapted to live in very different thermal environments.
| S-EPMC11007952 | biostudies-literature
Project description:Volvocine algae are a group of chlorophytes that together comprise a unique model for evolutionary and developmental biology. The species Chlamydomonas reinhardtii and Volvox carteri represent extremes in morphological diversity within the Volvocine clade. Chlamydomonas is unicellular and reflects the ancestral state of the group, while Volvox is multicellular and has evolved numerous innovations including germ-soma differentiation, sexual dimorphism, and complex morphogenetic patterning. The Chlamydomonas genome sequence has shed light on several areas of eukaryotic cell biology, metabolism and evolution, while the Volvox genome sequence has enabled a comparison with Chlamydomonas that reveals some of the underlying changes that enabled its transition to multicellularity, but also underscores the subtlety of this transition. Many of the tools and resources are in place to further develop Volvocine algae as a model for evolutionary genomics.
| S-EPMC4396658 | biostudies-literature
Project description:The evolution of anisogamy (the production of gametes of different size) is the first step in the establishment of sexual dimorphism, and it is a fundamental phenomenon underlying sexual selection. It is believed that anisogamy originated from isogamy (production of gametes of equal size), which is considered by most theorists to be the ancestral condition. Although nearly all plant and animal species are anisogamous, extant species of marine green algae exhibit a diversity of mating systems including both isogamy and anisogamy. Isogamy in marine green algae is of two forms: isogamy with extremely small gametes and isogamy with larger gametes. Based on disruptive selection for fertilization success and zygote survival (theory of Parker, Baker, and Smith), we explored how environmental changes can contribute to the evolution of such complex mating systems by analyzing the stochastic process in the invasion simulations of populations of differing gamete sizes. We find that both forms of isogamy can evolve from other isogamous ancestors through anisogamy. The resulting dimensionless analysis accounts for the evolutionary stability of all types of mating systems in marine green algae, even in the same environment. These results imply that evolutionary trajectories as well as the optimality of gametes/zygotes played an important role in the evolution of gamete size.
| S-EPMC3427103 | biostudies-literature
Project description:This study is the first determination of six chloroplast genomes of colonial volvocine algae, Colemanosphaera charkowiensis, Volvulina compacta, Pandorina colemaniae, Pandorina morum, Colemanosphaera angeleri, and Yamagishiella unicocca. Based on 55 chloroplast protein-coding genes, we compared the nonsynonymous (dN) and synonymous (dS) substitution rates between colonial volvocine algae and the other unicellular Chlamydomonadales species. When refer to the dN, we found 27 genes were significantly different, among them, 19 genes were significant higher in unicellular species (FDR-adjusted P < 0.05). When refer to the dS, we found 10 genes were significantly different, among them, 6 genes were significant higher in unicellular species (FDR-adjusted P < 0.05). Then we identified 14 putative fast-evolving genes and 11 putative positively selected genes of unicellular species, we analyzed the function of positively selected sites of the overlap genes of putative fast-evolving and positively selected genes, and found some sites were close to the important functional region of the proteins. Photosynthesis is the process to transform and store solar energy by chloroplast, it plays a vital role in the survival of algae, this study is the first to use the chloroplast genomes to analysis the evolutionary relationship between colonial and unicellular species in Chlamydomonadales. We found more genes have higher substitution rates in unicellular species and proposed that the fast-evolving and positively selected two genes, psbA and psbC, may help to improve the photosynthetic efficiency of unicellular species in Chlamydomonadales.
| S-EPMC6591512 | biostudies-literature
Project description:Evolutionary transitions in individuality (ETIs) underlie the watershed events in the history of life on Earth, including the origins of cells, eukaryotes, plants, animals, and fungi. Each of these events constitutes an increase in the level of complexity, as groups of individuals become individuals in their own right. Among the best-studied ETIs is the origin of multicellularity in the green alga Volvox, a model system for the evolution of multicellularity and cellular differentiation. Since its divergence from unicellular ancestors, Volvox has evolved into a highly integrated multicellular organism with cellular specialization, a complex developmental program, and a high degree of coordination among cells. Remarkably, all of these changes were previously thought to have occurred in the last 50-75 million years. Here we estimate divergence times using a multigene data set with multiple fossil calibrations and use these estimates to infer the times of developmental changes relevant to the evolution of multicellularity. Our results show that Volvox diverged from unicellular ancestors at least 200 million years ago. Two key innovations resulting from an early cycle of cooperation, conflict and conflict mediation led to a rapid integration and radiation of multicellular forms in this group. This is the only ETI for which a detailed timeline has been established, but multilevel selection theory predicts that similar changes must have occurred during other ETIs.
| S-EPMC2651347 | biostudies-literature
Project description:Colonial Volvocine Algae (CVA) are of great significance for biological evolution study, but little is presently known about their biogeographic distribution. Meanwhile, with the impact of climate change and human activities, their effects on the distribution and structures of CVA communities also remain largely unknown. Herein, the biogeography of CVA was investigated in the Yangtze River basin, 172 sampling sites were set up within a catchment area of 1,800,000 km2, and the distribution and community composition of CVA were studied using single-molecule real-time sequencing and metabarcoding technology based on the full-length 18S sequence. In 76 sampling sites, CVA was discovered in two families, eight genera, and nine species. Eudorina and Colemanosphaera were the main dominant genus. Based on the result of the random forest model and Eta-squared value, the distribution of CVA was significantly influenced by water temperature, altitude, and TP. CVA could be suitably distributed at an average water temperature of 22°C, an average TP concentration of 0.06 mg/L, and an altitude lower than 3,920 m. To assess the effects of anthropogenic pollution on the structures and co-occurrence patterns of CVA communities, we used a stress index calculated by 10 environmental factors to divide the CVA community into low and high pollution group. Network analysis showed that greater pollution levels would have a negative impact on the co-occurrence patterns and diversity of the CVA community. Finally, to study the scientific distribution of CVA under current and future climate change scenarios, we analyzed the climate suitability regionalization of CVA with the maximum entropy model based on 19 climatic factors and four climate scenarios from 2021 to 2040 published by CMIP6. Our results reveal the suitable areas of CVA, and temperature is an important environmental factor affecting the distribution of CVA. With the change of climate in the future, the Three Gorges Reservoir Area, Chaohu Lake, and Taihu Lake are still highly suitable areas for CVA, but the habitat of CVA may be fragmented, and more thorough temporal surveys and sampling of the sediment or mud are needed to investigate the fragmentation of CVA.
| S-EPMC9910701 | biostudies-literature
Project description:Somatic cellular differentiation plays a critical role in the transition from unicellular to multicellular life, but the evolution of its genetic basis remains poorly understood. By definition, somatic cells do not reproduce to pass on genes and so constitute an extreme form of altruistic behaviour. The volvocine green algae provide an excellent model system to study the evolution of multicellularity and somatic differentiation. In Volvox carteri, somatic cell differentiation is controlled by the regA gene, which is part of a tandem duplication of genes known as the reg cluster. Although previous work found the reg cluster in divergent Volvox species, its origin and distribution in the broader group of volvocine algae has not been known. Here, we show that the reg cluster is present in many species without somatic cells and determine that the genetic basis for soma arose before the phenotype at the origin of the family Volvocaceae approximately 200 million years ago. We hypothesize that the ancestral function was involved in regulating reproduction in response to stress and that this function was later co-opted to produce soma. Determining that the reg cluster was co-opted to control somatic cell development provides insight into how cellular differentiation, and with it greater levels of complexity and individuality, evolves.
| S-EPMC5540444 | biostudies-literature
Project description:Outcrossing and self-fertilization are fundamental strategies of sexual reproduction, each with different evolutionary costs and benefits. Self-fertilization is thought to be an evolutionary "dead-end" strategy, beneficial in the short term but costly in the long term, resulting in self-fertilizing species that occupy only the tips of phylogenetic trees. Here, we use volvocine green algae to investigate the evolution of self-fertilization. We use ancestral-state reconstructions to show that self-fertilization has repeatedly evolved from outcrossing ancestors and that multiple reversals from selfing to outcrossing have occurred. We use three phylogenetic metrics to show that self-fertilization is not restricted to the tips of the phylogenetic tree, a finding inconsistent with the view of self-fertilization as a dead-end strategy. We also find no evidence for higher extinction rates or lower speciation rates in selfing lineages. We find that self-fertilizing species have significantly larger colonies than outcrossing species, suggesting the benefits of selfing may counteract the costs of increased size. We speculate that our macroevolutionary results on self-fertilization (i.e., non-tippy distribution, no decreased diversification rates) may be explained by the haploid-dominant life cycle that occurs in volvocine algae, which may alter the costs and benefits of selfing.
| S-EPMC5796843 | biostudies-literature