RNA-Seq reveals divergent gene expression between larvae with contrasting trophic modes in the poecilogonous polychaete Boccardia wellingtonensis

The polychaete Boccardia wellingtonensis is a poecilogonous species that produces different larval types. Females may lay Type I capsules, in which only planktotrophic larvae are present, or Type III capsules that contain planktotrophic and adelphophagic larvae as well as nurse eggs. While planktotrophic larvae do not feed during encapsulation, adelphophagic larvae develop by feeding on nurse eggs and on other larvae inside the capsules and hatch at the juvenile stage. Previous works have not found differences in the morphology between the two larval types; thus, the factors explaining contrasting feeding abilities in larvae of this species are still unknown. In this paper, we use a transcriptomic approach to study the cellular and genetic mechanisms underlying the different larval trophic modes of B. wellingtonensis. By using approximately 624 million high-quality reads, we assemble the de novo transcriptome with 133,314 contigs, coding 32,390 putative proteins. We identify 5221 genes that are up-regulated in larval stages compared to their expression in adult individuals. The genetic expression profile differed between larval trophic modes, with genes involved in lipid metabolism and chaetogenesis over expressed in planktotrophic larvae. In contrast, up-regulated genes in adelphophagic larvae were associated with DNA replication and mRNA synthesis.

Geographic contingency, not species sorting, dominates macroevolutionary dynamics in an extinct clade of neogastropods (Volutospina; Volutidae)

Rates of speciation and extinction are often linked to many ecological factors, traits (emergent and nonemergent) such as environmental tolerance, body size, feeding type, and geographic range. Marine gastropods in particular have been used to examine the role of larval dispersal in speciation. However, relatively few studies have been conducted placing larval modes in species-level phylogenetic context. Those that have, have not incorporated fossil data, while landmark macroevolutionary studies on fossil clades have not considered both phylogenetic context and net speciation (speciation–extinction) rates. This study utilizes Eocene volutid Volutospina species from the U.S. Gulf Coastal Plain and the Hampshire Basin, U.K., to explore the relationships among larval mode, geographic range, and duration. Based on the phylogeny of these Volutospina, we calculated speciation and extinction rates in order to compare the macroevolutionary effects of larval mode. Species with planktotrophic larvae had a median duration of 9.7 Myr, which compared significantly to 4.7 Myr for those with non-planktotrophic larvae. Larval mode did not significantly factor into geographic-range size, but U.S. and U.K. species do differ, indicating a locality-specific component to maximum geographic-range size. Non-planktotrophs (NPTs)were absent among the Volutospina species during the Paleocene–early Eocene. The relative proportions of NPTs increased in the early middle Eocene, and the late Eocene was characterized by disappearance of planktotrophs (PTs). The pattern of observed lineage diversity shows an increasing preponderance of NPTs; however, this is clearly driven by a dramatic extinction of PTs, rather than higher NPT speciation rates during the late Eocene. This study adds nuance to paleontology's understanding of the macroevolutionary consequences of larval mode.

Analysis of the juvenile shell of Lingula anatina (Brachiopoda: Linguliformea) provides insight into the evolution of life cycles of fossil brachiopods

Inferences on the development and morphology of extinct brachiopods must be informed by the ontogeny and shell ornamentation of extant brachiopods. Although the adult shells of extant brachiopods are well studied, detailed descriptions of the embryonic and juvenile shells of extant lingulides are lacking. Here, we describe in detail the shells of juveniles of Lingula anatina Lamarck, 1801 from Vietnam and the Republic of the Philippines. The following previously unknown properties of the lingulide shell are described: (1) a distinct border between the protegulum and the brephic shell; (2) drapes that develop on both the protegulum and brephic shell; and (3) the notched anterior margin of the brephic shell. The drapes and cogs on the brephic shell may be caused by the formation of setal follicles during the planktonic stage. Specimens of L. anatina from the Philippines have larger brephic shells than those from Vietnam, probably because the former have a longer planktonic stage. Based on comparisons of the first-formed shells of extant brachiopods with published data on fossil brachiopods, we suggest that the life cycle of extant lingulides, in which planktotrophic juveniles with a shell hatch from the egg envelope, is the most evolutionarily advanced brachiopod life cycle and appeared in the early Silurian. We suggest criteria for determining the type of life cycle based on the structure of the first-formed shell of brachiopods. Finally, we consider hypothetical scenarios of life cycles of fossil brachiopods, including true planktotrophic larvae in the Cambrian linguliforms.

Plasticity and Artificial Selection for Developmental Mode in a Poecilogonous Sea Slug

Developmental mode describes the means by which larvae are provisioned with the nutrients they need to proceed through development and typically results in a trade-off between offspring size and number. The sacoglossan sea slug Alderia willowi exhibits intraspecific variation for developmental mode (= poecilogony) that is environmentally modulated with populations producing more yolk-feeding (lecithotrophic) larvae during the summer, and more planktonic feeding (planktotrophic) larvae in the winter. I found significant family level variation in the reaction norms between 17 maternal families of A. willowi when reared in low (16 ppt) versus high (32 ppt) salinity. I documented a significant response to selection for lecithotrophic larvae, the proportion of which increased 32% after three generations of selection in high salinity, and 18% after 2 generations in low salinity (realized heritability: 0.365 ± 0.024). The slope of the reaction norm was maintained following one generation of selection for lecithotrophy and one generation of selfing. The rapid response to selection favoring one developmental mode may speak to the rarity of intraspecific variation for developmental mode, which could fix for one mode over another much more readily than has generally been assumed from studies of less plastic organisms.

Ancestral form and function of larval feeding structures are retained during development of non-planktotrophic gastropods

Mode of development (MOD) is a key feature that influences the rate and direction of evolution of marine invertebrates. Although many groups include species with different MODs, the evolutionary loss of feeding larvae is thought to be irreversible as the complex structures used for larval feeding and swimming are lost, reduced, or modified in many species lacking feeding larvae. This view is largely based on observations of echinoderms. Phylogenetic analysis suggests that feeding larvae have been re-gained in at least one species of calyptraeid gastropod. Further, its sister species has retained the velum, the structure used for larval feeding and swimming. Here, we document velar morphology and function in calyptraeids with 4 different MODs. Embryos of Crepidula navicella, Crepidula atrasolea, Bostrycapulus aculeatus, Bostrycapulus odites, Bostrycapulus urraca, Crepipatella dilatata, Crepipatella occulta, Crucibulum quiriquinae and Crepidula coquimbensis all hatch as crawling juveniles, yet only Crepidula coquimbensis does not make a well-formed velum during intracapsular development. The velar dimensions of 6 species with non-planktotrophic development were similar to those of planktotrophic species, while the body sizes were significantly larger. All of the species studied were able to capture and ingest particles from suspension, but several non-planktotrophic species may ingest captured particles only occasionally. Video footage suggests that some species with adelphophagic direct development capture but frequently fail to ingest particles compared to species with the other MODs. Together these lines of evidence show that, among calyptraeids at least, species that lack planktotrophic larvae often retain the structures and functions necessary to successfully capture and ingest particles, reducing the barriers to the re-evolution of planktotrophy.

Geosesarma mirum, a new species of semi-terrestrial sesarmid crab (Crustacea, Decapoda, Brachyura) from central Taiwan

A new species of semi-terrestrial sesarmid crab of the genus Geosesarma De Man, 1892, is described from central Taiwan. Geosesarmamirumsp. nov. is distinct in possessing a strong transverse crest on the inner surface of the male chela and a diagnostic male first gonopod which is relatively long and stout, with the distal chitinous part broad and spatuliform. Like most Geosesarma species, G.mirumsp. nov. has large eggs and direct development, contrasting with the only other species known from Taiwan, G.hednon Ng, Liu and Schubart, 2004, which has small eggs and planktotrophic larvae.

Role of the larval feeding morphology and digestive enzyme activity in the early development of the polychaete Boccardia wellingtonensis

In marine invertebrates, the modes of development at early stages are related to the type and capacity of larval feeding to achieve growth. Therefore, studying the factors that determine larval feeding strategies can help to understand the diversity of life histories and evolution of marine invertebrates. The polychaete Boccardia wellingtonensis is a poecilogonous species that encapsulates and incubates its offspring. This species produces two types of larvae: (1) larvae that do not feed within the capsule and hatch as planktotrophic larvae (indirect development), and (2) adelphophagic larvae that feed on nurse eggs and other larvae inside the capsule to hatch as advanced larvae or juveniles (direct development). Otherwise, the larval types are indistinguishable at the same stage of development. The non-apparent morphological differences between both types of larvae suggest that other factors are influencing their feeding behavior. This work studied the potential role of the activity of 19 digestive enzymes on the different feeding capacities of planktotrophic and adelphophagic larvae of B. wellingtonensis. Also, differences in larval feeding structures and the larval capacity to feed from intracapsular fluid were evaluated by electron and fluorescence microscopy. Results showed that both types of larvae present similar feeding structures and had the capacity to ingest intracapsular fluid protein. Adelphophagic larvae showed overall the highest activities of digestive enzymes. Significant differences between larval types were observed in nine enzymes related to the use of internal and external nutritional sources. Given that larval feeding is closely related to larval development in species with encapsulation, this work supports that the study of the digestive enzymatic machinery of larvae may contribute to understanding the evolution of developmental modes.

The natural history of Calyptraea aurita (Reeve, 1859) from Southern Chile (Gastropoda, Calyptraeidae)

Hard bottom communities of the Reloncaví Estuary and adjacent areas, Region de los Lagos, Chile (42°S), were studied between 2008 and 2011. All hard substrates between the lower intertidal and 25 m depth were dominated by the calyptraeid gastropods,CrepipatelladilatataandC.fecunda. Epibenthic coverage of the hard bottoms markedly decreased further down with the exception of vertical cliffs. In a depth range between 26 to 48 m repeatedly dense patches of another calyptraeid species,Calyptraeaaurita(Reeve, 1859), were observed. Densities reached up to 1475 individuals m-2and covered up to 50 % of the rock surfaces. In shallower depthsC.auritawas not present. However, despite its huge abundance,C.auritahas not been documented for more than 150 years in the southeastern Pacific, being described superficially by Reeve, through only shell characteristics. Here, we redescribe and compare it with other members of the family Calyptraeidae through characteristics of shell, radula, and soft parts, including also details of the egg mass and intracapsular development of their embryos. Males were mobile and females sessile. Shell size ranged from 6.6 to 12.4 mm for immature individuals, from 10.6 to 24.9 mm for males, 15.1 to 25.9 mm for intersex individuals, and from 21.0 to 39.6 mm for females. Up to three individuals stacked together were found, always presenting a female at the base with up to a maximum of two male individuals above. Laboratory studies demonstrated thatC.auritahas an indirect larval development, liberating planktotrophic larvae with a bilobed ciliated velum into the water column. A transplantation experiment demonstrated that survival, growth, and reproduction ofC.auritais also possible in depths shallower than its normal distribution. The geographic distribution ofC.aurita, was previously only known as being from Valparaíso (33°S) and is now extended down to the Reloncaví Sound (41°S).

Phenotypic Plasticity of Feeding Structures in Marine Invertebrate Larvae

Nearly three decades ago, biologists discovered that planktotrophic larvae of sea urchins can alter the size of their ciliated feeding structures in response to the concentration of food (i.e., unicellular algae). In the years since, this response has become one of the best-studied examples of phenotypic plasticity in marine organisms. Researchers have found that this form of plasticity occurs widely among different types of feeding larvae in several phyla, and involves energetic trade-offs with a suite of correlated life history characters. Furthermore, investigators have recently started to unravel the genetic and molecular mechanisms underlying this plasticity. We review the literature on feeding-structure plasticity in marine invertebrate larvae. We highlight the diversity of species and variety of experimental designs and statistical methodologies, summarize research findings to draw more general conclusions, and target promising directions for future research.

Origin and Diversity of Marine Larvae

The origin of larvae has been much discussed, but the most plausible theory is the “terminal addition theory,” which proposes that the larvae originated when a benthic stage was added to the ancestral holoplanktonic life cycle, with the planktonic stage retained as the larva. Marine larvae show an astonishing morphological and ecological variation. Planktotrophic larvae are found in many smaller or larger lineages, and characteristic types—such as the trochophore of many annelids and molluscs, the cyphonautes of some bryozoans, the actinotrocha of most phoronids, the pluteus larvae of most echinoderms, and the tornaria of some enteropneusts—are familiar members of the plankton. These larvae show different types of ciliary filter feeding: trochophores have downstream-collecting, cyphonautes and actinotrocha have ciliary-sieving, and pluteus and actiunotrocha have upstream-collecting feeding. Crustacean larvae show a variety of feeding mechanisms. Lecithotrophic larvae are found in all phyla. A panorama of marine larvae is presented.