Habitat segregation of plate phenotypes in a rapidly expanding population of three-spined stickleback

Declines of large predatory fish due to overexploitation are restructuring food webs across the globe. It is now becoming evident that restoring these altered food webs requires addressing not only ecological processes, but evolutionary ones as well, because human-induced rapid evolution may in turn affect ecological dynamics. We studied the potential for niche differentiation between different plate armor phenotypes in a rapidly expanding population of a small prey fish, the three-spined stickleback (Gasterosteus aculeatus). In the central Baltic Sea, three-spined stickleback abundance has increased dramatically during the past decades. The increase in this typical mesopredator has restructured near-shore food webs, increased filamentous algal blooms, and threatens coastal biodiversity. Time-series data covering 22 years show that the increase coincides with a decline in the number of juvenile perch (Perca fluviatilis), the most abundant predator of stickleback along the coast. We investigated the distribution of different stickleback plate armor phenotypes depending on latitude, environmental conditions, predator and prey abundances, nutrients, and benthic production; and described the stomach content of the stickleback phenotypes using metabarcoding. We found two distinct lateral armor plate phenotypes of stickleback, incompletely and completely plated. The proportion of incompletely plated individuals increased with increasing benthic production and decreasing abundances of adult perch. Metabarcoding showed that the stomach content of the completely plated individuals more often contained invertebrate herbivores (amphipods) than the incompletely plated ones. Since armor plates are defense structures favored by natural selection in the presence of fish predators, the phenotype distribution suggests that a novel low-predation regime favors stickleback with less armor. Our results suggest that morphological differentiation of the three-spined stickleback has the potential to affect food web dynamics and influence the persistence and resilience of the stickleback take-over in the Baltic Sea.Peer reviewe

The rise of the three-spined stickleback – eco-evolutionary consequences of a mesopredator release

Declines of large predatory fish due to overexploitation are restructuring food webs across the globe. It is now becoming evident that restoring these altered food webs requires addressing not only ecological processes, but evolutionary ones as well, because human-induced rapid evolution may in turn affect ecological dynamics. In the central Baltic Sea, abundances of the mesopredatory fish, the three-spined stickleback (Gasterosteus aculeatus), have increased dramatically during the past decades. Time-series data covering 22 years show that this increase coincides with a decline in the number of juvenile perch (Perca fluviatilis), the most abundant predator of stickleback along the coast. We studied the interaction between evolutionary and ecological effects of this mesopredator take-over, by surveying the armour plate morphology of stickleback and the structure of the associated food web. First, we investigated the distribution of different stickleback phenotypes depending on predator abundances and benthic production; and described the stomach content of the stickleback phenotypes using metabarcoding. Second, we explored differences in the relation between different trophic levels and benthic production, between bays where the relative abundance of fish was dominated by stickleback or not; and compared this to previous cage-experiments to support causality of detected correlations. We found two distinct lateral armour plate phenotypes of stickleback, incompletely and completely plated. The proportion of incompletely plated individuals increased with increasing benthic production and decreasing abundances of adult perch. Stomach content analyses showed that the completely plated individuals had a stronger preference for invertebrate herbivores (amphipods) than the incompletely plated ones. In addition, predator dominance interacted with ecosystem production to determine food web structure and the propagation of a trophic cascade: with increasing production, biomass accumulated on the first (macroalgae) and third (stickleback) trophic levels in stickleback-dominated bays, but on the second trophic level (invertebrate herbivores) in perch-dominated bays. Since armour plates are defence structures favoured by natural selection in the presence of fish predators, the phenotype distribution suggest that a novel low-predation regime favours sticklebacks with less armour. Our results indicate that an interaction between evolutionary and ecological effects of the stickleback take-over has the potential to affect food web dynamics

Could coastal plants in western Amazonia be relicts of past marine incursions?

The rainforests of Amazonia comprise some of the most biologically diverse ecosystems on Earth. Despite this high biodiversity, little is known about how landscape changes that took place in deep history have affected the assembly of its species, and whether the impact of such changes on biodiversity can still be observed. Here, we present a hypothesis to explain our observation that plants typical of Neotropical coastal habitats also occur in western Amazonia, in some cases thousands of kilometres away from the coast. Evidence on their current distribution, dispersal biology and divergence times estimated from molecular phylogenies suggest that these plants may be the legacy of the large marine‐influenced embayment that dominated the area for millions of years in the Neogene. We hypothesize that coastal plants dispersed along the shores of this embayment and persisted as inland relicts after the marine incursion(s) retreated, probably with the aid of changes in soil conditions caused by the deposition of marine sediments. This dispersal corridor may also have facilitated the colonization of coastal environments by Amazonian lineages. These scenarios could imply an unexpected coastal source that has contributed to Amazonia's high floristic diversity and led to disjunct distributions across the Neotropics. We highlight the need for future studies and additional evidence to validate and shed further light on this potentially important pattern.</p

Towards a multisensor station for automated biodiversity monitoring

Rapid changes of the biosphere observed in recent years are caused by both small and large scale drivers, like shifts in temperature, transformations in land-use, or changes in the energy budget of systems. While the latter processes are easily quantifiable, documentation of the loss of biodiversity and community structure is more difficult. Changes in organismal abundance and diversity are barely documented. Censuses of species are usually fragmentary and inferred by often spatially, temporally and ecologically unsatisfactory simple species lists for individual study sites. Thus, detrimental global processes and their drivers often remain unrevealed. A major impediment to monitoring species diversity is the lack of human taxonomic expertise that is implicitly required for large-scale and fine-grained assessments. Another is the large amount of personnel and associated costs needed to cover large scales, or the inaccessibility of remote but nonetheless affected areas. To overcome these limitations we propose a network of Automated Multisensor stations for Monitoring of species Diversity (AMMODs) to pave the way for a new generation of biodiversity assessment centers. This network combines cutting-edge technologies with biodiversity informatics and expert systems that conserve expert knowledge. Each AMMOD station combines autonomous samplers for insects, pollen and spores, audio recorders for vocalizing animals, sensors for volatile organic compounds emitted by plants (pVOCs) and camera traps for mammals and small invertebrates. AMMODs are largely self-containing and have the ability to pre-process data (e.g. for noise filtering) prior to transmission to receiver stations for storage, integration and analyses. Installation on sites that are difficult to access require a sophisticated and challenging system design with optimum balance between power requirements, bandwidth for data transmission, required service, and operation under all environmental conditions for years. An important prerequisite for automated species identification are databases of DNA barcodes, animal sounds, for pVOCs, and images used as training data for automated species identification. AMMOD stations thus become a key component to advance the field of biodiversity monitoring for research and policy by delivering biodiversity data at an unprecedented spatial and temporal resolution. (C) 2022 Published by Elsevier GmbH on behalf of Gesellschaft fur Okologie

Rapid progress on the vertebrate tree of life

<p>Abstract</p> <p>Background</p> <p>Among the greatest challenges for biology in the 21st century is inference of the tree of life. Interest in, and progress toward, this goal has increased dramatically with the growing availability of molecular sequence data. However, we have very little sense, for any major clade, of how much progress has been made in resolving a full tree of life and the scope of work that remains. A series of challenges stand in the way of completing this task but, at the most basic level, progress is limited by data: a limited fraction of the world's biodiversity has been incorporated into a phylogenetic analysis. More troubling is our poor understanding of what fraction of the tree of life is understood and how quickly research is adding to this knowledge. Here we measure the rate of progress on the tree of life for one clade of particular research interest, the vertebrates.</p> <p>Results</p> <p>Using an automated phylogenetic approach, we analyse all available molecular data for a large sample of vertebrate diversity, comprising nearly 12,000 species and 210,000 sequences. Our results indicate that progress has been rapid, increasing polynomially during the age of molecular systematics. It is also skewed, with birds and mammals receiving the most attention and marine organisms accumulating far fewer data and a slower rate of increase in phylogenetic resolution than terrestrial taxa. We analyse the contributors to this phylogenetic progress and make recommendations for future work.</p> <p>Conclusions</p> <p>Our analyses suggest that a large majority of the vertebrate tree of life will: (1) be resolved within the next few decades; (2) identify specific data collection strategies that may help to spur future progress; and (3) identify branches of the vertebrate tree of life in need of increased research effort.</p

The enigmatic mitochondrial genome of Rhabdopleura compacta (Pterobranchia) reveals insights into selection of an efficient tRNA system and supports monophyly of Ambulacraria

<p>Abstract</p> <p>Background</p> <p>The Hemichordata comprises solitary-living Enteropneusta and colonial-living Pterobranchia, sharing morphological features with both Chordata and Echinodermata. Despite their key role for understanding deuterostome evolution, hemichordate phylogeny is controversial and only few molecular data are available for phylogenetic analysis. Furthermore, mitochondrial sequences are completely lacking for pterobranchs. Therefore, we determined and analyzed the complete mitochondrial genome of the pterobranch <it>Rhabdopleura compacta </it>to elucidate deuterostome evolution. Thereby, we also gained important insights in mitochondrial tRNA evolution.</p> <p>Results</p> <p>The mitochondrial DNA of <it>Rhabdopleura compacta </it>corresponds in size and gene content to typical mitochondrial genomes of metazoans, but shows the strongest known strand-specific mutational bias in the nucleotide composition among deuterostomes with a very GT-rich main-coding strand. The order of the protein-coding genes in <it>R. compacta </it>is similar to that of the deuterostome ground pattern. However, the protein-coding genes have been highly affected by a strand-specific mutational pressure showing unusual codon frequency and amino acid composition. This composition caused extremely long branches in phylogenetic analyses. The unusual codon frequency points to a selection pressure on the tRNA translation system to codon-anticodon sequences of highest versatility instead of showing adaptations in anticodon sequences to the most frequent codons. Furthermore, an assignment of the codon AGG to Lysine has been detected in the mitochondrial genome of <it>R. compacta</it>, which is otherwise observed only in the mitogenomes of some arthropods. The genomes of these arthropods do not have such a strong strand-specific bias as found in <it>R. compacta </it>but possess an identical mutation in the anticodon sequence of the tRNA_Lys.</p> <p>Conclusion</p> <p>A strong reversed asymmetrical mutational constraint in the mitochondrial genome of <it>Rhabdopleura compacta </it>may have arisen by an inversion of the replication direction and adaptation to this bias in the protein sequences leading to an enigmatic mitochondrial genome. Although, phylogenetic analyses of protein coding sequences are hampered, features of the tRNA system of <it>R. compacta </it>support the monophyly of Ambulacraria. The identical reassignment of AGG to Lysine in two distinct groups may have occurred by convergent evolution in the anticodon sequence of the tRNA_Lys.</p

Evolution of a Core Gene Network for Skeletogenesis in Chordates

The skeleton is one of the most important features for the reconstruction of vertebrate phylogeny but few data are available to understand its molecular origin. In mammals the Runt genes are central regulators of skeletogenesis. Runx2 was shown to be essential for osteoblast differentiation, tooth development, and bone formation. Both Runx2 and Runx3 are essential for chondrocyte maturation. Furthermore, Runx2 directly regulates Indian hedgehog expression, a master coordinator of skeletal development. To clarify the correlation of Runt gene evolution and the emergence of cartilage and bone in vertebrates, we cloned the Runt genes from hagfish as representative of jawless fish (MgRunxA, MgRunxB) and from dogfish as representative of jawed cartilaginous fish (ScRunx1–3). According to our phylogenetic reconstruction the stem species of chordates harboured a single Runt gene and thereafter Runt locus duplications occurred during early vertebrate evolution. All newly isolated Runt genes were expressed in cartilage according to quantitative PCR. In situ hybridisation confirmed high MgRunxA expression in hard cartilage of hagfish. In dogfish ScRunx2 and ScRunx3 were expressed in embryonal cartilage whereas all three Runt genes were detected in teeth and placoid scales. In cephalochordates (lancelets) Runt, Hedgehog and SoxE were strongly expressed in the gill bars and expression of Runt and Hedgehog was found in endo- as well as ectodermal cells. Furthermore we demonstrate that the lancelet Runt protein binds to Runt binding sites in the lancelet Hedgehog promoter and regulates its activity. Together, these results suggest that Runt and Hedgehog were part of a core gene network for cartilage formation, which was already active in the gill bars of the common ancestor of cephalochordates and vertebrates and diversified after Runt duplications had occurred during vertebrate evolution. The similarities in expression patterns of Runt genes support the view that teeth and placoid scales evolved from a homologous developmental module

OrthoSelect: a protocol for selecting orthologous groups in phylogenomics

Background: Phylogenetic studies using expressed sequence tags (EST) are becoming a standard approach to answer evolutionary questions. Such studies are usually based on large sets of newly generated, unannotated, and error-prone EST sequences from different species. A first crucial step in EST-based phylogeny reconstruction is to identify groups of orthologous sequences. From these data sets, appropriate target genes are selected, and redundant sequences are eliminated to obtain suitable sequence sets as input data for tree-reconstruction software. Generating such data sets manually can be very time consuming. Thus, software tools are needed that carry out these steps automatically. Results: We developed a flexible and user-friendly software pipeline, running on desktop machines or computer clusters, that constructs data sets for phylogenomic analyses. It automatically searches assembled EST sequences against databases of orthologous groups (OG), assigns ESTs to these predefined OGs, translates the sequences into proteins, eliminates redundant sequences assigned to the same OG, creates multiple sequence alignments of identified orthologous sequences and offers the possibility to further process this alignment in a last step by excluding potentially homoplastic sites and selecting sufficiently conserved parts. Our software pipeline can be used as it is, but it can also be adapted by integrating additional external programs. This makes the pipeline useful for non-bioinformaticians as well as to bioinformatic experts. The software pipeline is especially designed for ESTs, but it can also handle protein sequences. Conclusion: OrthoSelect is a tool that produces orthologous gene alignments from assembled ESTs. Our tests show that OrthoSelect detects orthologs in EST libraries with high accuracy. In the absence of a gold standard for orthology prediction, we compared predictions by OrthoSelect to a manually created and published phylogenomic data set. Our tool was not only able to rebuild the data set with a specificity of 98%, but it detected four percent more orthologous sequences. Furthermore, the results OrthoSelect produces are in absolut agreement with the results of other programs, but our tool offers a significant speedup and additional functionality, e.g. handling of ESTs, computing sequence alignments, and refining them. To our knowledge, there is currently no fully automated and freely available tool for this purpose. Thus, OrthoSelect is a valuable tool for researchers in the field of phylogenomics who deal with large quantities of EST sequences. OrthoSelect is written in Perl and runs on Linux/Mac OS X

Acoelomorpha: earliest branching bilaterians or deuterostomes?

The Acoelomorpha is an animal group comprised by nearly 400 species of misleadingly inconspicuous flatworms. Despite this, acoelomorphs have been at the centre of a heated debate about the origin of bilaterian animals for 150 years. The animal tree of life has undergone major changes during the last decades, thanks largely to the advent of molecular data together with the development of more rigorous phylogenetic methods. There is now a relatively robust backbone of the animal tree of life. However, some crucial nodes remain contentious, especially the node defining the root of Bilateria. Some studies situate Acoelomorpha (and Xenoturbellida) as the sister group of all other bilaterians, while other analyses group them within the deuterostomes which instead suggests that the last common bilaterian ancestor directly gave rise to deuterostomes and protostomes. The resolution of this node will have a profound impact on our understanding of animal/bilaterian evolution. In particular, if acoelomorphs are the sister group to Bilateria, it will point to a simple nature for the first bilaterian. Alternatively, if acoelomorphs are deuterostomes, this will imply that they are the result of secondary simplification. Here, we review the state of this question and provide potential ways to solve this long-standing issue. Specifically, we argue for the benefits of (1) obtaining additional genomic data from acoelomorphs, in particular from taxa with slower evolutionary rates; (2) the development of new tools to analyse the data; and (3) the use of metagenomics or metatranscriptomics data. We believe the combination of these three approaches will provide a definitive answer as to the position of the acoelomorphs in the animal tree of life

Evolution of a New Function by Degenerative Mutation in Cephalochordate Steroid Receptors

Gene duplication is the predominant mechanism for the evolution of new genes. Major existing models of this process assume that duplicate genes are redundant; degenerative mutations in one copy can therefore accumulate close to neutrally, usually leading to loss from the genome. When gene products dimerize or interact with other molecules for their functions, however, degenerative mutations in one copy may produce repressor alleles that inhibit the function of the other and are therefore exposed to selection. Here, we describe the evolution of a duplicate repressor by simple degenerative mutations in the steroid hormone receptors (SRs), a biologically crucial vertebrate gene family. We isolated and characterized the SRs of the cephalochordate Branchiostoma floridae, which diverged from other chordates just after duplication of the ancestral SR. The B. floridae genome contains two SRs: BfER, an ortholog of the vertebrate estrogen receptors, and BfSR, an ortholog of the vertebrate receptors for androgens, progestins, and corticosteroids. BfSR is specifically activated by estrogens and recognizes estrogen response elements (EREs) in DNA; BfER does not activate transcription in response to steroid hormones but binds EREs, where it competitively represses BfSR. The two genes are partially coexpressed, particularly in ovary and testis, suggesting an ancient role in germ cell development. These results corroborate previous findings that the ancestral steroid receptor was estrogen-sensitive and indicate that, after duplication, BfSR retained the ancestral function, while BfER evolved the capacity to negatively regulate BfSR. Either of two historical mutations that occurred during BfER evolution is sufficient to generate a competitive repressor. Our findings suggest that after duplication of genes whose functions depend on specific molecular interactions, high-probability degenerative mutations can yield novel functions, which are then exposed to positive or negative selection; in either case, the probability of neofunctionalization relative to gene loss is increased compared to existing models