skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Resolving Marine–Freshwater Transitions by Diatoms Through a Fog of Gene Tree Discordance
Abstract Despite the obstacles facing marine colonists, most lineages of aquatic organisms have colonized and diversified in freshwaters repeatedly. These transitions can trigger rapid morphological or physiological change and, on longer timescales, lead to increased rates of speciation and extinction. Diatoms are a lineage of ancestrally marine microalgae that have diversified throughout freshwater habitats worldwide. We generated a phylogenomic data set of genomes and transcriptomes for 59 diatom taxa to resolve freshwater transitions in one lineage, the Thalassiosirales. Although most parts of the species tree were consistently resolved with strong support, we had difficulties resolving a Paleocene radiation, which affected the placement of one freshwater lineage. This and other parts of the tree were characterized by high levels of gene tree discordance caused by incomplete lineage sorting and low phylogenetic signal. Despite differences in species trees inferred from concatenation versus summary methods and codons versus amino acids, traditional methods of ancestral state reconstruction supported six transitions into freshwaters, two of which led to subsequent species diversification. Evidence from gene trees, protein alignments, and diatom life history together suggest that habitat transitions were largely the product of homoplasy rather than hemiplasy, a condition where transitions occur on branches in gene trees not shared with the species tree. Nevertheless, we identified a set of putatively hemiplasious genes, many of which have been associated with shifts to low salinity, indicating that hemiplasy played a small but potentially important role in freshwater adaptation. Accounting for differences in evolutionary outcomes, in which some taxa became locked into freshwaters while others were able to return to the ocean or become salinity generalists, might help further distinguish different sources of adaptive mutation in freshwater diatoms. [hemiplasy; homoplasy; phylogenomics; salinity, Thalassiosirales.]  more » « less
Award ID(s):
1651087
PAR ID:
10431211
Author(s) / Creator(s):
; ; ; ; ;
Publisher / Repository:
Oxford University Press
Date Published:
Journal Name:
Systematic Biology
ISSN:
1063-5157
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Piganeau, Gwenael (Ed.)
    Abstract Numerous factors shape the evolution of protein-coding genes, including shifts in the strength or type of selection following gene duplications or changes in the environment. Diatoms and other silicifying organisms use a family of silicon transporters (SITs) to import dissolved silicon from the environment. Freshwaters contain higher silicon levels than oceans, and marine diatoms have more efficient uptake kinetics and less silicon in their cell walls, making them better competitors for a scarce resource. We compiled SITs from 37 diatom genomes to characterize shifts in selection following gene duplications and marine–freshwater transitions. A deep gene duplication, which coincided with a whole-genome duplication, gave rise to two gene lineages. One of them (SIT1–2) is present in multiple copies in most species and is known to actively import silicon. These SITs have evolved under strong purifying selection that was relaxed in freshwater taxa. Episodic diversifying selection was detected but not associated with gene duplications or habitat shifts. In contrast, genes in the second SIT lineage (SIT3) were present in just half the species, the result of multiple losses. Despite conservation of SIT3 in some lineages for the past 90–100 million years, repeated losses, relaxed selection, and low expression highlighted the dispensability of SIT3, consistent with a model of deterioration and eventual loss due to relaxed selection on SIT3 expression. The extensive but relatively balanced history of duplications and losses, together with paralog-specific expression patterns, suggest diatoms continuously balance gene dosage and expression dynamics to optimize silicon transport across major environmental gradients. 
    more » « less
  2. Synopsis This series of papers highlights research into how biological exchanges between salty and freshwater habitats have transformed the biosphere. Life in the ocean and in freshwaters have long been intertwined; multiple major branches of the tree of life originated in the oceans and then adapted to and diversified in freshwaters. Similar exchanges continue to this day, including some species that continually migrate between marine and fresh waters. The series addresses key themes of transitions, transformations, and current threats with a series of questions: When did major colonizations of fresh waters happen? What physiographic changes facilitated transitions? What organismal characteristics facilitate colonization? Once a lineage has colonized freshwater, how frequently is there a return to the sea? Have transitions impelled diversification? How do organisms adapt physiologically to changes in halohabitat, and are such adaptive changes predictable? How do marine and freshwater taxa differ in morphology? How are present-day global changes in the environment influencing halohabitat and how are organisms contending with them? The purpose of the symposium and the papers in this volume is to integrate findings at multiple levels of biological organization and from disparate fields, across biological and geoscience disciplines. 
    more » « less
  3. Environmental transitions, such as the salinity divide separating marine and fresh waters, shape biodiversity over both shallow and deep timescales, opening up new niches and creating opportunities for accelerated speciation and adaptive radiation. Understanding the genetics of environmental adaptation is central to understanding how organisms colonise and subsequently diversify in new habitats. We used time‐resolved transcriptomics to contrast the hyposalinity stress responses of two diatoms. Skeletonema marinoi has deep marine ancestry but has recently invaded brackish waters. Cyclotella cryptica has deep freshwater ancestry and can withstand a much broader salinity range. Skeletonema marinoi is less adept at mitigating even mild salinity stress compared to Cyclotella cryptica, which has distinct mechanisms for rapid mitigation of hyposaline stress and long‐term growth in low salinity. We show that the cellular mechanisms underlying low salinity tolerance, which has allowed diversification across freshwater habitats worldwide, includes elements that are both conserved and variable across the diatom lineage. The balance between ancestral and lineage‐specific environmental responses in phytoplankton have shaped marine–freshwater transitions on evolutionary timescales and, on contemporary timescales, will affect which lineages survive and adapt to changing ocean conditions. 
    more » « less
  4. Abstract The salinity gradient separating marine and freshwater environments represents a major ecological divide for microbiota, yet the mechanisms by which marine microbes have adapted to and ultimately diversified in freshwater environments are poorly understood. Here, we take advantage of a natural evolutionary experiment: the colonization of the brackish Baltic Sea by the ancestrally marine diatom Skeletonema marinoi. To understand how diatoms respond to low salinity, we characterized transcriptomic responses of acclimated S. marinoi grown in a common garden. Our experiment included eight strains from source populations spanning the Baltic Sea salinity cline. Gene expression analysis revealed that low salinities induced changes in the cellular metabolism of S. marinoi, including upregulation of photosynthesis and storage compound biosynthesis, increased nutrient demand, and a complex response to oxidative stress. However, the strain effect overshadowed the salinity effect, as strains differed significantly in their response, both regarding the strength and the strategy (direction of gene expression) of their response. The high degree of intraspecific variation in gene expression observed here highlights an important but often overlooked source of biological variation associated with how diatoms respond to environmental change. 
    more » « less
  5. Abstract Evolutionary transitions between marine and freshwater ecosystems have occurred repeatedly throughout the phylogenetic history of fishes. The theory of ecological opportunity predicts that lineages that colonize species-poor regions will have greater potential for phenotypic diversification than lineages invading species-rich regions. Thus, transitions between marine and freshwaters may promote phenotypic diversification in trans-marine/freshwater fish clades. We used phylogenetic comparative methods to analyze body size data in nine major fish clades that have crossed the marine/freshwater boundary. We explored how habitat transitions, ecological opportunity, and community interactions influenced patterns of phenotypic diversity. Our analyses indicated that transitions between marine and freshwater habitats did not drive body size evolution, and there are few differences in body size between marine and freshwater lineages. We found that body size disparity in freshwater lineages is not correlated with the number of independent transitions to freshwaters. We found a positive correlation between body size disparity and overall species richness of a given area, and a negative correlation between body size disparity and diversity of closely related species. Our results indicate that the diversity of incumbent freshwater species does not restrict phenotypic diversification, but the diversity of closely related taxa can limit body size diversification. Ecological opportunity arising from colonization of novel habitats does not seem to have a major effect in the trajectory of body size evolution in trans-marine/freshwater clades. Moreover, competition with closely related taxa in freshwaters has a greater effect than competition with distantly related incumbent species. 
    more » « less