Phylogenetic relationships and the timing of evolutionary events are essential for understanding evolution on longer time scales. Cheilostome bryozoans are a group of ubiquitous, species-rich, marine colonial organisms with an excellent fossil record but lack phylogenetic relationships inferred from molecular data. We present genome-skimmed data for 395 cheilostomes and combine these with 315 published sequences to infer relationships and the timing of key events among c. 500 cheilostome species. We find that named cheilostome genera and species are phylogenetically coherent, rendering fossil or contemporary specimens readily delimited using only skeletal morphology. Our phylogeny shows that parental care in the form of brooding evolved several times independently but was never lost in cheilostomes. Our fossil calibration, robust to varied assumptions, indicates that the cheilostome lineage and parental care therein could have Paleozoic origins, much older than the first known fossil record of cheilostomes in the Late Jurassic.
Kelp species are ecologically-important habitat-formers in coastal marine ecosystems, where they alter environmental conditions and promote local biodiversity by providing complex biogenic habitat for an array of associated organisms. While it is widely accepted that kelps harbour significant biodiversity, our current understanding of spatiotemporal variability in kelp-associated assemblages and the key environmental drivers of variability patterns remains limited. Here we examined the influence of ocean temperature and wave exposure on the structure of faunal assemblages associated with the holdfasts of Laminaria hyperborea, the dominant habitat-forming kelp in the northeast Atlantic. We sampled holdfasts from 12 kelp-dominated open-coast sites nested within four regions across the UK, spanning ~9° in latitude and ~2.7° C in mean sea surface temperature. Overall, holdfast assemblages were highly diverse, with 261 taxa representing 11 phyla recorded across the study. We examined patterns of spatial variability for sessile and mobile taxa separately, and documented high variability between regions, between sites within regions, and between replicate holdfasts for both assemblage types. Mobile assemblage structure was more strongly linked to temperature variability than sessile assemblage structure, which was principally structured by site-level variability in factors such as wave exposure. Patterns in the structure of both biogenic habitat and associated assemblages did not vary predictably along a latitudinal gradient in temperature, indicating that other processes acting across multiple spatial and temporal scales are important drivers of assemblage structure. Overall, kelp holdfasts in the UK supported high levels of diversity, that were similar to other kelp-dominated systems globally and comparable to those recorded for other vegetated marine habitats (i.e. seagrass beds), which are perhaps more widely recognised for their high biodiversity value.
Polyembryony–the production of multiple cloned embryos from a single fertilised egg–is a seemingly paradoxical combination of reproductive modes that nevertheless persists in diverse taxa. We document features of polyembryony in the Cyclostomata (Bryozoa)–an ancient order of modular colonial marine invertebrates–that suggest a substantial reduction in the paradoxical nature of this enigmatic reproductive mode. Firstly, we provide molecular evidence for polyembryony in three exemplar species, supporting the widely cited inference that polyembryony characterises the entire order. Secondly, genotyping demonstrates protracted release of cloned offspring from the primary embryo in a given gonozooid (chamber for embryonic incubation), thus exposing the same genotype to changing environmental conditions over time. Finally, we confirm that each gonozooid produces a distinct genotype, with each primary embryo being the result of a separate fertilisation event. We hypothesise that the sustained release of one or a few genotypes against varying environmental conditions achieves levels of risk-spreading similar to those in organisms that release multiple, unique genotypes at a single time. We argue that polyembryony, specifically with the production of a large number of progeny per fertilisation event, has been favoured in the Cyclostomata over long geological periods.
Foundation species elevate local biodiversity and underpin critical ecological processes and functions. Kelp species are distributed along ~25% of the world’s coastlines, where they serve as foundation species in intertidal and subtidal habitats. As well as ameliorating environmental conditions and producing organic matter, they provide biogenic habitat for a vast array of associated organisms. Here, we investigated patterns of diversity and structure in assemblages associated with the stipe of the kelp Laminaria hyperborea in the NE Atlantic. Stipes were sampled at 4 study regions (with 3 sites nested within each region) in the UK, spanning ~9° of latitude. Stipe-associated communities were highly diverse (134 species) and abundant (16-4532 ind. stipe-1), with no obvious sequential shift in diversity or overall trends in abundance/biomass of assemblages with latitude. However, we observed high degrees of variability between sites from the same region and individuals within sites, indicating that processes working across smaller spatial scales were more important than those at regional scales. While we observed high between-site variability in assemblage structure, regional differences were also evident. Most notably, sites within our southernmost region (southern England) were largely devoid of amphipods that dominated all other regions. This study highlights the important role of L. hyperborea in elevating biodiversity at local to regional scales through a facilitative interaction. Moreover, given that L. hyperborea forests may be increasingly impacted by ocean warming, changes in coastal water quality and proposed exploitation, our study serves as an important benchmark against which to detect future changes.
Cheilostomata is the most diverse and ecologically dominant order of bryozoans living today. We apply a Bayesian framework to estimate macroevolutionary rates of cheilostomes since the Late Jurassic across four datasets: (I) manually curated genus ranges; (II) published text-mined genus ranges; (III) non-revised Paleobiology Database (PBDB) records; (IV) revised and augmented PBDB records. All datasets revealed increased origination rates in the Albian, and a twin K-Pg and Danian extinction rate peak. High origination rates in the Late Selandian-Ypresian in Dataset I indicate the onset of an ascophoran-grade radiation. Lineage-through-time plots confirm the macroevolutionary lag preceding the radiation of cheilostomes in the middle Cretaceous, and their renewed diversification in the late Paleocene and Eocene. A multivariate birth-death model indicates that origination rates are shaped by diversity-dependent dynamics coupled with a positive correlation with sea surface temperature, while extinction rates negatively correlate with sea level. Text-mined data provide broadly similar rate dynamics as manually curated data, although discrepancies could be attributed to the omission of key literature in Dataset II, and the inclusion of new published and unpublished data, and revised ranges in Dataset I. Revision and augmentation of PBDB occurrences were necessary to generate rate profiles akin to those of Datasets I and II and highlight the risks of using unedited occurrence data. Our results support the widely held assumption that diversification dynamics are controlled by both biotic and abiotic factors, and pave the way for integrating fossils with molecular phylogenies to study these processes in more detail.
1. Climate change can alter ecological communities both directly, by driving shifts in species distributions and abundances, and indirectly by influencing the strength and direction of species interactions. Within benthic marine ecosystems, foundation species such as canopy-forming macro-algae often underpin important cascades of facilitative interactions.2. We examined the wider impacts of climate-driven shifts in the relative abundances of foundation species within a temperate reef system, with particular focus on a habitat cascade whereby kelp facilitate epiphytic algae that, in turn, facilitate mobile invertebrates. Specifically, we tested whether the warm-water kelp Laminaria ochroleuca, which has proliferated in response to recent warming trends, facilitated a secondary habitat-former (epiphytic algae on stipes) and associated mobile invertebrates, to the same degree as the cold-water kelp Laminaria hyperborea.3. The facilitative interaction between kelp and stipe-associated epiphytic algae was dramatically weaker for the warm-water foundation species, leading to breakdown of a habitat cascade and impoverished associated faunal assemblages. On average, the warm-water kelp supported >250 times less epiphytic algae (by biomass) and >50 times fewer mobile invertebrates (by abundance) than the cold-water kelp. Moreover, by comparing regions of pre-and postrange expansion by L. ochroleuca, we found that warming-impacted kelp forests supported around half the biomass of epiphytic algae and one-fifth of the abundance of mobile invertebrates, per unit area, compared with unimpacted forests. We suggest that disruption to this facilitation cascade has the potential to
Many sessile, suspension-feeding marine invertebrates mate by spermcasting: aquatic sperm are spawned and gathered by conspecific individuals to fertilize eggs that are generally retained during development. In two phylogenetically distant examples, a cheilostome bryozoan and an aplousobranch ascidian, the receipt of allosperm has previously been shown to alter sex allocation by triggering female investment in eggs and brooding. Here we report experiments demonstrating that two species of cyclostome bryozoan also show restrained female investment in the absence of mating opportunity. In Tubulipora plumosa, the production of female zooids and progeny is much reduced in reproductive isolation. In Filicrisia geniculata, development of distinctive female zooids (gonozooids) begins but halts in the absence of mating opportunity, and no completed gonozooids or progeny result. Reduced female investment in the absence of a mate thus occurs in at least two orders of Bryozoa, but significant differences in detail exist and the evolutionary history within the phylum of the mechanism(s) by which female investment is initiated might be complex. The broadening taxonomic spectrum of examples where female investment appears restrained until allosperm becomes available may signify a general adaptive strategy among outcrossing modular animals, analogous to similarly adaptive sex allocation typical of many flowering plants.
Animal mitogenomes are typically devoid of introns. Here, we report the largest number of mitochondrial introns ever recorded from bilaterian animals. Mitochondrial introns were identified for the first time from the phylum Bryozoa. They were found in four species from three families (Order Cheilostomatida). A total of eight introns were found in the complete mitogenome of Exechonella vieirai, and five, 17 and 18 introns were found in the partial mitogenomes of Parantropora penelope, Discoporella cookae and Cupuladria biporosa, respectively. Intron-encoded protein domains reverse transcriptase and intron maturase (RVT-IM) were identified in all species. Introns in E. vieirai and P. penelope had conserved Group II intron ribozyme domains V and VI. Conserved domains were lacking from introns in D. cookae and C. biporosa, preventing their further categorization. Putative origins of metazoan introns were explored in a phylogenetic context, using an up-to-date alignment of mitochondrial RVT-IM domains. Results confirmed previous findings of multiple origins of annelid, placozoan and sponge RVT-IM domains and provided evidence for common intron donor sources across metazoan phyla. Our results corroborate growing evidence that some metazoans with regenerative abilities (i.e. placozoans, sponges, annelids and bryozoans) are susceptible to intron integration, most likely via horizontal gene transfer.
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