Genes with evidence of positive selection as potentially related to coloniality and the evolution of morphological features among the lophophorates and entoprocts

Abstract

Evolutionary mechanisms that underlie the origins of coloniality among organisms are diverse. Some animal colonies may be comprised strictly of clonal individuals formed from asexual budding or comprised of a chimera of clonal and sexually produced individuals that fuse secondarily. This investigation focuses on select members of the lophophorates and entoprocts whose evolutionary relationships remain enigmatic even in the age of genomics. Using transcriptomic data sets, two coloniality‐based hypotheses are tested in a phylogenetic context to find candidate genes showing evidence of positive selection and potentially convergent molecular signatures among solitary species and taxa‐forming colonies from aggregate groups or clonal budding. Approximately 22% of the 387 orthogroups tested showed evidence of positive selection in at least one of the three branch‐site tests (CODEML, BUSTED, and aBSREL). Only 12 genes could be reliably associated with a developmental function related to traits linked with coloniality, neuroanatomy, or ciliary fields. Genes testing for both positive selection and convergent molecular characters include orthologues of Radial spoke head, Elongation translation initiation factors, SEC13, and Immediate early response gene5. Maximum likelihood analyses included here resulted in tree topologies typical of other phylogenetic investigations based on wider genomic information. Further genomic and experimental evidence will be needed to resolve whether a solitary ancestor with multiciliated cells that formed aggregate groups gave rise to colonial forms in bryozoans (and perhaps the entoprocts) or that the morphological differences exhibited by phoronids and brachiopods represent trait modifications from a colonial ancestor.

Phylogenomics reveals deep relationships and diversification within phylactolaemate bryozoans

“…A range of non-phylactolaemate bryozoans: three cyclostomes, six ctenostomes and five cheilostomes were also included along with two phoronids and two brachiopods as outgroups. Thirty-two transcriptomes, including 31 bryozoans and one phoronid, were newly generated while 12 transcriptomes were sampled from publicly available data as either raw sequence reads ( Fredericella sultana 5, 6 & 7 [ 27 ]; Flustrellidra corniculata and Heteropora pacifica [ 28 ]; Laqueus californicus and Membranipora membranacea [ 29 ]; Phoronis vancouverensis [ 30 ]; Schizoporella errata and Watersipora subtorquata [ 31 ]) or assembled transcriptomes ( Bugulina stolonifera [ 32 ] and Lingula anatina [ 33 ]); details of the specimens, sources of publicly available sequences and GenBank Bioproject accession number are given in electronic supplementary material, table S1. Digital vouchers for most species of plumatellids and fredericellids are available on Dryad digital repository.…”

Evolution of animal coloniality and modularity: Emerging themes

“…For example, to explain the evolution of polymorphs (castes) in social insects (i.e., division of labor among altruistic nonreproductive and reproductive individuals) early research developed kin selection theory—and the concept of inclusive fitness (Queller & Strassmann, 1998)⁠, which has more recently been expanded to include selection acting at the different hierarchical levels of the colony (i.e., multilevel selection theory) (Nowak et al, 2010)⁠. Because colonial modular animals are generally clonal and maximally related—beside exceptions stressed in Santagata (2021, This issue in this issue)—recent research show that selection of colony level traits and multilevel selection theory may provide a useful evolutionary framework to understand the evolution of polymorphs (Simpson, 2021, This issue; Simpson et al, 2020)⁠, as well as other evolutionary conflicts (Blackstone, 2021, This issue)⁠.…”

“…As a result, R. Strathmann raises many questions and hypotheses about the consequence of brooding, or in some cases not‐brooding, for the life history and reproduction of the different taxa (Strathmann, 2021, This issue)⁠.Unsatisfied with the all the attention given to genetic relatedness and inclusive fitness as major evolutionary drivers for the evolution of polymorphism in eusocial insects, C. Simpson—in the fourth article (research article)—develops a new theoretical framework to propose a new hypothesis that he terms the “life‐history ratchet.” The focus of this hypothesis is placed on the evolution of new body types (i.e., polymorph types) as a way to release colonies from ancestral life history strategy constraints, generated by the reduced numbers of body types. Mechanisms of colonial development Dias et al (2021, This issue)⁠ (research article) contribute with an elegant ecological study and experimental transplantation in a marina; they document phenotypic responses of bryozoan colonies to heteregeneous environments that affect overall morphology of the colonies, as well as the composition of polymorphic zooids in the colony, demonstrating a trade‐off between clonal growth and defense (density of avicularia).By comparing developmental mechanisms of budding, Alié et al (2021, This issue)⁠ (review) do a superb job to highlight the different cells and tissues that have been coopted in budding in the different groups of ascidians, suggesting a highly plastic nature of cell and tissues in this phylum. They raise the importance of tunicate diverse mechanisms of budding, as a goldmine to study evolutionary plastic developmental traits.By using positive selection tests on orthologous genes, followed by independent gene tree analyses, using several transcriptomes of entoprocts, bryozoans, and phoronids, Santagata (2021, This issue)⁠ (research article) identifies a pool of genes potentially related to the convergent evolution of coloniality among entoprocts and bryozoans, and probably also the “colonial‐like” (highly aggregate) phoronids. Signaling in colony regeneration and patterning In a laboratory experimental setting, Luz et al (2021, This issue)⁠ (research article) report predominant effects of fragment size in the process of regeneration in a group of invasive colonial dendrophylliid corals and show that Wnt and FGF—signaling pathways known to function in regeneration—are expressed during whole‐body regeneration in Tubastraea coccinea , a calcified anthozoan species fostered by the authors as a laboratory model.Cartwright et al (2021, This issue)⁠ (review) review variation and plasticity of colony forms in the hydrozoans and hypothesize that Wnt signaling may play an important role in colony patterning and morphology. From unicellular to multicellular colonies Cellular behaviors and developmental mechanisms that regulate the formation of colonies in aggregative bacteria have evolved multiple times. To understand the evolution of multicellular colonies and the developmental dynamics involved in their emergence, Guzmán‐Herrera et al (2021, This issue)⁠ (commentary and perspective) use events of morphogenesis of the fruiting body in Myxococcus xanthus —which corresponds to the multicellular aggregative stage of the bacterium—to integrate a dynamic patterning module framework with a systems biology framework, namely using network motifs.…”

“…By using positive selection tests on orthologous genes, followed by independent gene tree analyses, using several transcriptomes of entoprocts, bryozoans, and phoronids, Santagata (2021, This issue)⁠ (research article) identifies a pool of genes potentially related to the convergent evolution of coloniality among entoprocts and bryozoans, and probably also the “colonial‐like” (highly aggregate) phoronids.…”

Polyzoa is back: The effect of complete gene sets on the placement of Ectoprocta and Entoprocta

“…The application of the phylogenomic approach yields contradictory results: Some studies still favor Lophophorata monophyly (15,(31)(32)(33)(34)(35), while many researches abandon the Lophophorata concept (1,3,4,14,(36)(37)(38)(39)(40)(41). The placement of the lophotrochozoan groups in different studies is also contradictory (Fig.…”