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Peters, A. F.

Publications and source records attributed to Peters, A. F..

10 recordsLinked to original sources

Haplotype tagging sheds light on speciation between two divergent cryptic species of the brown algae Ectocarpus

Understanding how genome-wide divergence translates to barriers to gene flow is a central question in speciation research, particularly in marine environments where interconnected habitats frequently accommodate cryptic diversity. Using linked-read whole-genome data from the brown alga Ectocarpus, we investigated genome-wide reproductive isolation between two cryptic brown algal species E. siliculosus and E. crouaniorum across replicated hybrid zones in Europe and Chile. We first uncover deep genetic structure within E. crouaniorum, revealing a more intricate species complex than previously recognized. Despite this complexity, we found parallel patterns of asymmetric introgression that emerged independently in Europe and Chile, where we detected both, F1 and low-level introgressed individuals. However, the specific lineage pairs involved in hybridization depended on local demographic history. Demographic modeling further indicated that reproductive isolation strengthens gradually with divergence time and differs markedly between geographic regions, with ongoing asymmetric gene flow even between lineage pairs where hybrids were not detected in the field. In all cases, the genomic landscape of hybridization is consistent with a polygenic, genome-wide barrier to gene flow rather than a few large-effect regions. Our results show that cryptic speciation in brown algae is driven by repeatable, regionally parallel architectures of genome-wide reproductive isolation which is shaped by ecological and demographic context.

evolutionary biology↗

Origin and evolutionary trajectories of brown algal sex chromosomes

Sex chromosomes fall into three classes: XX/XY, ZW/ZZ and U/V systems. The rise, evolution and demise of U/V systems has remained an evolutionary enigma. Here, we analyse genomes spanning the entire brown algal phylogeny to decipher their sex-determination evolutionary history. U/V sex chromosomes emerged between 450 and 224 million years ago, when a region containing the pivotal male-determinant MIN located in a discrete region in proto-U and proto-V chromosomes ceased recombining. Over time, nested inversions led to step-wise expansions of the sex locus, accompanying increasing morphological complexity and sexual differentiation of brown seaweeds. Unlike XX/XY and ZW/ZZ, brown algal U/V evolve mainly by gene gain, showing minimal degeneration. They are structurally dynamic and act as genomic cradles fostering the birth of new genes, potentially from ancestrally non coding sequences. Our analyses demonstrate that hermaphroditism arose from ancestral males that acquired U-specific genes by ectopic recombination, and that in the transition from a U/V to an XX/XY system, V-specific genes moved down the genetic hierarchy of sex determination. Both events lead to the demise of U and V and erosion of their specific genomic characteristics. Taken together, our findings offer a comprehensive model of U/V sex chromosome evolution.

evolutionary biology↗

The baseless mutant links protein phosphatase 2A with basal cell identity in the brown alga Ectocarpus

The first mitotic division of the initial cell is a key event in all multicellular organisms and is usually concomitant with the establishment of major developmental axes and cell fates. The brown alga Ectocarpus has a haploid-diploid life cycle that involves the development of two multicellular and independent generations, the sporophyte and the gametophyte. Each generation deploys a distinct developmental program autonomously from an initial cell, whose first cell division sets up the future body pattern. Here, we show that mutations in the BASELESS (BAS) gene result in multiple cellular defects during the first division of the initial cell and subsequently failure to produce basal structures (rhizoids and prostrate filaments) during both generations of the life cycle. Cloning-by-sequencing revealed that BAS encodes a type B" regulatory subunit of protein phosphatase 2A, and transcriptomic analysis of early developmental stages uncovered potential effector genes involved in setting up basal cell fate in this organism. The bas mutant phenotype is very similar to that observed in the distag (dis) mutants, which lack a functional TBCCd1 protein, at both the cellular and morphological levels. The high level of similarity of the dis and bas mutant phenotypes indicate that TBCCd1 and PP2A are two critical components of the cellular machinery that regulates the division of the initial cell and mediates the establishment of basal cell fate in the developing thallus.

developmental biology↗

A partially sex-reversed giant kelp sheds light into the mechanisms of sexual differentiation in a UV sexual system

In UV sexual systems, sex is determined during the haploid phase of the life cycle and males have a V chromosome whereas females have a U chromosome. Previous work in the brown algal model Ectocarpus revealed that the V chromosome has a dominant role in male sex determination and suggested that the female developmental program may occur by default, triggered in the absence of the male master sex determination gene(s). Here, we describe the identification of a genetically male giant kelp strain presenting phenotypic features typical of a female, despite lacking the U-specific region. The conversion to the female developmental program is however incomplete, because gametes of this feminised male are unable to produce the sperm-attracting pheromone lamoxirene. We identify the transcriptomic patterns underlying the male and female specific developmental programs, and reveal the faster evolutionary rates of male-biased genes compared to female-biased and unbiased genes. Moreover, we show that the phenotypic feminisation of the variant strain is associated with both feminisation and de-masculinisation of gene expression patterns. Importantly, the feminisation phenotype was associated with the dramatic downregulation of two V-specific genes including a candidate sex-determining gene on the V-specific region. Our results reveal the transcriptional changes associated with sexual differentiation in a UV system with marked sexual dimorphism, and contribute to disentangling the role of sex-linked genes and autosomal gene expression in the initiation of the male and female developmental programs. Overall, the data presented here imply that the U-specific region in the giant kelp is not required to initiate the female developmental program, but is critical to produce fully functional eggs, arguing against the idea that female is the default sex in this species.

evolutionary biology↗

Revisiting Australian Ectocarpus subulatus (Phaeophyceae) from the Hopkins River: distribution, abiotic environment, and associated microbiota

Ectocarpus is a genus of common marine brown algae. In 1995 a strain of Ectocarpus was isolated from Hopkins River Falls, Victoria, Australia, constituting one of few available freshwater or nearly freshwater brown algae, and the only one belonging to Ectocarpus. It has since been used as a model to study acclimation and adaptation to low salinities and the role of its microbiota in these processes. However, little is known about the distribution of this strain or whether it represents a stable population. Furthermore, its microbiota may have been impacted by the long period of cultivation.\n\nTwenty-two years after the original finding we searched for Ectocarpus in the Hopkins River and surrounding areas. We found individuals with ITS and cox1 sequences identical to the original isolate at three sites upstream of Hopkins River Falls, but none at the original isolation site. The osmolarity of the water at these sites ranged from 74-170 mOsmol, and it was rich in sulfate. The diversity of bacteria associated with the algae in situ was approximately one order of magnitude higher than in previous studies of the original laboratory culture, and 95 alga-associated bacterial strains were isolated from E. subulatus filaments on site. In particular, Planctomycetes were abundant in situ but rare in the laboratory-cultured strain.\n\nOur results confirm that E. subulatus has stably colonized the Hopkins River, and the newly isolated algal and bacterial strains offer new possibilities to study the adaptation of Ectocarpus to low salinity and its interactions with its microbiome.

plant biology↗

Evolution of life cycles and reproductive traits: insights from 1 the brown algae

Brown algae are characterized by a remarkable diversity of life cycles, sexual systems, and reproductive modes, and these traits seem to be very labile across the whole group. This diversity makes them ideal models to test existing theories on the evolution of alternation between generations, and to examine correlations between life cycle and reproductive life history traits. In this study, we investigate the dynamics of trait evolution for four life-history traits: life cycle, sexual system, level of gamete dimorphism and gamete parthenogenetic capacity. We assign states to up to 70 species in a multi-gene phylogeny of brown algae, and use maximum likelihood and Bayesian analyses of correlated evolution, taking phylogeny into account, to test for correlations between life history traits and sexual systems, and to investigate the sequence of trait acquisition. Our analyses are consistent with the prediction that diploid growth may evolve because it allows the complementation of deleterious mutations, and that haploid sex determination is ancestral in relation to diploid sex determination. However, the idea that increased zygotic and diploid growth is associated with increased sexual dimorphism is not supported by our analysis. Finally, it appears that in the brown algae isogamous species evolved from anisogamous ancestors.

evolutionary biology↗

A key role for UV sex chromosomes in the regulation of parthenogenesis in the brown alga Ectocarpus

AO_SCPLOWBSTRACTC_SCPLOWAlthough evolutionary transitions from sexual to asexual reproduction are frequent in eukaryotes, the genetic bases of these shifts remain largely elusive. Here, we used classic quantitative trait analysis, combined with genomic and transcriptomic information to dissect the genetic basis of asexual, parthenogenetic reproduction in the brown alga Ectocarpus. We found that parthenogenesis is controlled by the sex locus, together with two additional autosomal loci, highlight the key role of the sex chromosome as a major regulator of asexual reproduction. Importantly, we identify several negative effects of parthenogenesis on male fitness, but also different fitness effects between parthenogenesis and life cycle generations, supporting the idea that parthenogenesis may be under both sexual selection and generation/ploidally-antagonistic selection. Overall, our data provide the first empirical illustration, to our knowledge, of a trade-off between the haploid and diploid stages of the life cycle, where distinct parthenogenesis alleles have opposing effects on sexual and asexual reproduction and may contribute to the maintenance of genetic variation. These types of fitness trade-offs have profound evolutionary implications in natural populations and may structure life history evolution in organisms with haploid-diploid life cycles.

evolutionary biology↗

Convergent recruitment of life cycle regulators to direct sporophyte development in two eukaryotic supergroups

Three amino acid loop extension homeodomain transcription factors (TALE HD TFs) act as life cycle regulators in green algae and land plants. In mosses these regulators are required for the deployment of the sporophyte developmental program. We demonstrate that mutations in either of two TALE HD TF genes, OUROBOROS or SAMSARA, in the brown alga Ectocarpus result in conversion of the sporophyte generation into a gametophyte. The OUROBOROS and SAMSARA proteins heterodimerise in a similar manner to TALE HD TF life cycle regulators in the green lineage. These observations demonstrate that TALE-HD-TF-based life cycle regulation systems have an extremely ancient origin, and that these systems have been independently recruited to regulate sporophyte developmental programs in at least two different complex multicellular eukaryotic supergroups, Archaeplastida and Chromalveolata.

plant biology↗

The genome of Ectocarpus subulatus highlights unique mechanisms for stress tolerance in brown algae

Brown algae are multicellular photosynthetic stramenopiles that colonize marine rocky shores worldwide. Ectocarpus sp. Ec32 has been established as a genomic model for brown algae. Here we present the genome and metabolic network of the closely related species, Ectocarpus subulatus Kutzing, which is characterized by high abiotic stress tolerance. Since their separation, both strains show new traces of viral sequences and the activity of large retrotransposons, which may also be related to the expansion of a family of chlorophyll-binding proteins. Further features suspected to contribute to stress tolerance include an expanded family of heat shock proteins, the reduction of genes involved in the production of halogenated defence compounds, and the presence of fewer cell wall polysaccharide-modifying enzymes. Overall, E. subulatus has mainly lost members of gene families down-regulated in low salinities, and conserved those that were up-regulated in the same condition. However, 96% of genes that differed between the two examined Ectocarpus species, as well as all genes under positive selection, were found to encode proteins of unknown function. This underlines the uniqueness of brown algal stress tolerance mechanisms as well as the significance of establishing E. subulatus as a comparative model for future functional studies.

genomics↗

Rapid turnover of life-cycle-related genes in the brown algae

BackgroundSexual life cycles in eukaryotes involve a cyclic alternation between haploid and diploid phases. While most animals possess a diploid life cycle, plants and algae alternate between multicellular haploid (gametophyte) and diploid (sporophyte) generations. In many algae, gametophytes and sporophytes are independent and free living, and may present dramatic phenotypic differences. The same shared genome can therefore be subject to different, even conflicting, selection pressures in each of the life cycle generations. Here, we have analysed the nature and extent of genome-wide generation-biased gene expression in four species of brown algae with contrasting levels of dimorphism between life cycle generations, in order to assess the potential role of generation-specific selection in shaping patterns of gene expression and divergence.\n\nResultsWe show that the proportion of the transcriptome that is generation-biased is associated with the level of phenotypic dimorphism between the life cycle stages. Importantly, our data reveals a remarkably high turnover rate for life-cycle-related gene sets across the brown algae and highlights the importance not only of co-option of regulatory programs from one generation to the other but also a key role for newly emerged, lineage-specific genes in the evolution of the gametophyte and sporophyte developmental programs in this major eukaryotic group. Moreover, we show that generation-biased genes display distinct evolutionary modes, with gametophyte-biased genes evolving rapidly at the coding sequence level whereas sporophyte-biased genes exhibit changes in their patterns of expression.\n\nConclusionOur analysis uncovers the characteristics, expression patterns and evolution of generation-biased genes and underline the selective forces that shape this previously underappreciated source of phenotypic diversity.

evolutionary biology↗