Elucidating relationships among early animal lineages has been difficult, and recent phylogenomic analyses place Ctenophora sister to all other extant animals, contrary to the traditional view of Porifera as the earliest-branching animal lineage. To date, phylogenetic support for either ctenophores or sponges as sister to other animals has been limited and inconsistent among studies. Lack of agreement among phylogenomic analyses using different data and methods obscures how complex traits, such as epithelia, neurons, and muscles evolved. A consensus view of animal evolution will not be accepted until datasets and methods converge on a single hypothesis of early metazoan relationships and putative sources of systematic error (e.g., longbranch attraction, compositional bias, poor model choice) are assessed. Here, we investigate possible causes of systematic error by expanding taxon sampling with eight novel transcriptomes, strictly enforcing orthology inference criteria, and progressively examining potential causes of systematic error while using both maximum-likelihood with robust data partitioning and Bayesian inference with a site-heterogeneous model. We identified ribosomal protein genes as possessing a conflicting signal compared with other genes, which caused some past studies to infer ctenophores and cnidarians as sister. Importantly, biases resulting from elevated compositional heterogeneity or elevated substitution rates are ruled out. Placement of ctenophores as sister to all other animals, and sponge monophyly, are strongly supported under multiple analyses, herein.phylogenomics | Metazoa | Ctenophora | Porifera | Cnidaria R esolving relationships among extant lineages at the base of the metazoan tree is integral to understanding evolution of complex animal traits, including nervous systems and gastrulation. Historically, sponges and placozoans, both of which have relatively simple body plans and lack neurons, have been considered to diverge from other animals earlier than ctenophores, cnidarians, and bilaterians (1). Phylogenomic studies have resulted in controversial hypotheses placing either Placozoa (Fig. 1A) (2), ctenophores (ctenophore-sister hypothesis) (Fig. 1B) (3-7), or a clade of ctenophores and sponges (Fig. 1C) (6) as sister to all remaining animals. Others (7-10) have claimed nontraditional findings resulted from systematic error and argued for traditional placement of sponges as sister to all remaining animals (Eumetazoa, or Porifera-sister hypothesis) (Fig. 1D) and a sister relationship between ctenophores and cnidarians (Coelenterata) (Fig. 1D). Limited statistical support for various hypotheses and conflict among, and even within studies, has undermined confidence in our understanding of early animal evolution. Basal metazoan relationships must be resolved with greater consistency before a consensus viewpoint is widely accepted.Long-branch attraction (LBA) (11), which occurs when two divergent lineages are artificially inferred as related because of substitutional saturation (11), is p...
Ctenophora, compromising approximately 200 described species, is an important lineage for understanding metazoan evolution and is of great ecological and economic importance. Ctenophore diversity includes species with unique colloblasts used for prey capture, smooth and striated muscles, benthic and pelagic lifestyles, and locomotion with ciliated paddles or muscular propulsion. However, ancestral states of traits are debated and relationships among many lineages are unresolved. Here, using 27 newly sequenced ctenophore transcriptomes, publicly available data, and methods to control systematic error we establish the placement of Ctenophora as the sister group to all other animals and refine phylogenetic relationships within ctenophores. Molecular clock analyses suggest modern ctenophore diversity originated approximately 350MYA ± 88 MY, conflicting with previous hypotheses of approximately 65 MYA. We recover Euplokamis dunlapae, a species with striated muscles, as the sister lineage to other sampled ctenophores. Ancestral state reconstruction shows the most recent common ancestor of extant ctenophores was pelagic, possessed tentacles, was bioluminescent, and did not have separate sexes. Our results imply at least two transitions from a pelagic to a benthic lifestyle within Ctenophora, suggesting such transitions were more common in animal diversification than appreciated.
This is the first American Fisheries Society conservation assessment of freshwater gastropods (snails) from Canada and the United States by the Gastropod Subcommittee (Endangered Species Committee). This review covers 703 species representing 16 families and 93 genera, of which 67 species are considered extinct, or possibly extinct, 278 are endangered, 102 are threatened, 73 are vulnerable, 157 are currently stable, and 26 species have uncertain taxonomic status. Of the entire fauna, 74% of gastropods are imperiled (vulnerable, threatened, endangered) or extinct, which exceeds imperilment levels in fishes (39%) and crayfishes (48%) but is similar to that of mussels (72%). Comparison of modern to background extinction rates reveals that gastropods have the highest modern extinction rate yet observed, 9,539 times greater than background rates. Gastropods are highly susceptible to habitat loss and degradation, particularly narrow endemics restricted to a single spring or short stream reaches. Compilation of this review was hampered by a paucity of current distributional information and taxonomic uncertainties. Although research on several fronts including basic biology, physiology, conservation strategies, life history, and ecology are needed, systematics and curation of museum collections and databases coupled with comprehensive status surveys (geographic limits, threat identification) are priorities.
As phylogenetic datasets have increased in size, site-heterogeneous substitution models such as CAT-F81 and CAT-GTR have been advocated in favor of other models because they purportedly suppress long-branch attraction (LBA). These models are two of the most commonly used models in phylogenomics, and they have been applied to a variety of taxa, ranging from Drosophila to land plants. However, many arguments in favor of CAT models have been based on tenuous assumptions about the true phylogeny, rather than rigorous testing with known trees via simulation. Moreover, CAT models have not been compared to other approaches for handling substitutional heterogeneity such as data partitioning with site-homogeneous substitution models. We simulated amino acid sequence datasets with substitutional heterogeneity on a variety of tree shapes including those susceptible to LBA. Data were analyzed with both CAT models and partitioning to explore model performance; in total over 670,000 CPU hours were used, of which over 97% was spent running analyses with CAT models. In many cases, all models recovered branching patterns that were identical to the known tree. However, CAT-F81 consistently performed worse than other models in inferring the correct branching patterns, and both CAT models often overestimated substitutional heterogeneity. Additionally, reanalysis of two empirical metazoan datasets supports the notion that CAT-F81 tends to recover less accurate trees than data partitioning and CAT-GTR. Given these results, we conclude that partitioning and CAT-GTR perform similarly in recovering accurate branching patterns. However, computation time can be orders of magnitude less for data partitioning, with commonly used implementations of CAT-GTR often failing to reach completion in a reasonable time frame (i.e., for Bayesian analyses to converge). Practices such as removing constant sites and parsimony uninformative characters, or using CAT-F81 when CAT-GTR is deemed too computationally expensive, cannot be logically justified. Given clear problems with CAT-F81, phylogenies previously inferred with this model should be reassessed. [Data partitioning; phylogenomics, simulation, site-heterogeneity, substitution models.].
Imbalances in phosphorus (P) intake relative to demand negatively affect animal growth, but their consequences are less understood for vertebrates, in which bone represents a significant and potentially flexible pool of P. Flexibility in body-P content could buffer vertebrates from the effects of imbalances between P intake and demand, reducing the likelihood of a sharp stoichiometric ''knife-edge'' in the relationship between growth rate and diet-P level. We conducted a meta-analysis of published aquaculture experiments that tested effects of diet %P on fish growth rate (49 studies, 28 species) and body-P content (27 of the studies in the main data set, 20 species). Our meta-analysis revealed significant P limitation of growth, as well as significant negative effects of excess P on growth rate. Diet-P thresholds for these effects occurred at ecologically relevant levels (optimal diet-P of 1.2% 6 0.45%, mean 6 SD, under experimental conditions of high ration). Finally, the analysis also suggested a pattern of relatively shallow relationships between growth rate and diet-P level, coupled with surprisingly flexible body-P content in fishes. This result is consistent with fish using flexible body-P content (presumably mediated through bone P) to buffer imbalances between P intake and demand. Together, our results provide evidence for a relatively ''dull'' stoichiometric ''knife-edge'' in fishes, driven in part by flexible body-P content.
Within riverine systems, headwater populations are hypothesized to harbour higher amounts of genetic distinctiveness than populations in the main stem of a river and display increased genetic diversity in large, downstream habitats. However, these hypotheses were mostly developed with insects and fish, and they have not been tested on many invertebrate lineages. Pleuroceridae gastropods are of particular ecological importance to rivers of eastern North America, sometimes comprising over 90% of macroinvertebrate biomass. Yet, virtually nothing is known of pleurocerid landscape genetics, including whether genetic diversity follows predictions made by hypotheses developed on more mobile species. Moreover, the commonly repeated hypothesis that intraspecific morphological variation in gastropods results from ecophenotypic plasticity has not been well tested on pleurocerids. Using 2bRAD‐seq to discover single nucleotide polymorphisms, we show that the threatened, Cahaba River endemic pleurocerid, Leptoxis ampla, has limited gene flow among populations and that migration is downstream‐biased, conflicting with previous hypotheses. Both tributary and main stem populations harbour unique genomic profiles, and genetic diversity was highest in downstream populations. Furthermore, L. ampla shell morphology was more correlated with genetic differences among individuals and populations than habitat characteristics. We anticipate similar genetic and demographic patterns to be seen in other pleurocerids, and hypotheses about gene flow and population demographics that were based on more mobile taxa often, but not always, apply to freshwater gastropods. From a conservation standpoint, genetic structure of L. ampla populations suggests distinctive genetic diversity is lost with localized extirpation, a phenomenon common across the range of Pleuroceridae.
Deep‐sea tubeworms (Annelida, Siboglinidae) represent dominant species in deep‐sea chemosynthetic communities (e.g. hydrothermal vents and cold methane seeps) and occur in muddy sediments and organic falls. Siboglinids lack a functional digestive tract as adults, and they rely on endosymbiotic bacteria for energy, making them of evolutionary and physiological interest. Despite their importance, inferred evolutionary history of this group has been inconsistent among studies based on different molecular markers. In particular, placement of bone‐eating Osedax worms has been unclear in part because of their distinctive biology, including harbouring heterotrophic bacteria as endosymbionts, displaying extreme sexual dimorphism and exhibiting a distinct body plan. Here, we reconstructed siboglinid evolutionary history using 12 newly sequenced transcriptomes. We parsed data into three data sets that accommodated varying levels of missing data, and we evaluate effects of missing data on phylogenomic inference. Additionally, several multispecies‐coalescent approaches and Bayesian concordance analysis (BCA) were employed to allow for a comparison of results to a supermatrix approach. Every analysis conducted herein strongly supported Osedax being most closely related to the Vestimentifera and Sclerolinum clade, rather than Frenulata, as previously reported. Importantly, unlike previous studies, the alternative hypothesis that frenulates and Osedax are sister groups to one another was explicitly rejected by an approximately unbiased (AU) test. Furthermore, although different methods showed largely congruent results, we found that a supermatrix method using data partitioning with site‐homogenous models potentially outperformed a supermatrix method using the CAT‐GTR model and multispecies‐coalescent approaches when the amount of missing data varies in a data set and when taxa susceptible to LBA are included in the analyses.
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