Larval ecology and morphology in fossil gastropods

The shell of marine gastropods conserves and reflects early ontogeny, including embryonic and larval stages, to a high degree when compared with other marine invertebrates. Planktotrophic larval development is indicated by a small embryonic shell (size is also related to systematic placement) with little yolk followed by a multiwhorled shell formed by a free‐swimming veliger larva. Basal gastropod clades (e.g. Vetigastropoda) lack planktotrophic larval development. The great majority of Late Palaeozoic and Mesozoic ‘derived’ marine gastropods (Neritimorpha, Caenogastropoda and Heterobranchia) with known protoconch had planktotrophic larval development. Dimensions of internal moulds of protoconchs suggest that planktotrophic larval development was largely absent in the Cambrian and evolved at the Cambrian–Ordovician transition, mainly due to increasing benthic predation. The evolution of planktotrophic larval development offered advantages and opportunities such as more effective dispersal, enhanced gene flow between populations and prevention of inbreeding. Early gastropod larval shells were openly coiled and weakly sculptured. During the Mid‐ and Late Palaeozoic, modern tightly coiled larval shells (commonly with strong sculpture) evolved due to increasing predation pressure in the plankton. The presence of numerous Late Palaeozoic and Triassic gastropod species with planktotrophic larval development suggests sufficient primary production although direct evidence for phytoplankton is scarce in this period. Contrary to previous suggestions, it seems unlikely that the end‐Permian mass extinction selected against species with planktotrophic larval development. The molluscan classes with highest species diversity (Gastropoda and Bivalvia) are those which may have planktotrophic larval development. Extremely high diversity in such groups as Caenogastropoda or eulamellibranch bivalves is the result of high phylogenetic activity and is associated with the presence of planktotrophic veliger larvae in many members of these groups, although causality has not been shown yet. A new gastropod species and genus, Anachronistella peterwagneri, is described from the Late Triassic Cassian Formation; it is the first known Triassic gastropod with an openly coiled larval shell.     

Evolutionary links between reproductive morphology, ecology and mating behavior in opisthobranch gastropods

Sexual coevolution in morphological and behavioral traits has rarely been studied. Using phylogenetic analyses, we explore relationships between sexual characters based on a new molecular phylogeny of 33 opisthobranch taxa (Aglajidae and Gastropteridae). Our measurements of these simultaneous hermaphrodites include male and female reproductive anatomy, mating behavior, and spatial gregariousness. After phylogenetic correction, we found evidence for correlated evolution between male and female reproductive organs such as the size of the seminal fluid producing prostate gland and that of the sperm digesting bursa copulatrix. Our findings suggest that reproductive trait variation is mediated by sexual coevolution, where putatively manipulative male organs evolved in association with female organs involved in sperm selection. Furthermore, low gregariousness was associated with long, reciprocal copulations. We interpret this result as an adaptation to infrequent mate encounters, where it pays to mate longer with and presumably transfer more sperm to a rare partner. Several complex reproductive traits were repeatedly gained or lost across our phylogeny. This pattern is consistent with a scenario in which sexual selection generates dynamic coevolutionary cycles similar to those expected under sexual antagonism. We finally outline approaches for experimentally assessing the proposed functional links that underlie the evolutionary correlations revealed by our study.     

Trilobite larvae and larval ecology

Silicified trilobite faunas yield a well preserved and abundant record of early development in many taxa. Although their morphologies are well known, protaspid larvae are poorly understood in terms of trilobite life history and developmental biology. Two distinct morphologic types are recognized among the great diversity of protaspides studied; these are termed adult‐like and nonadult‐tike according to gross similarity to later developmental stages. Transitions between nonadult‐like and adult‐like morphologies are abrupt, occurring between successsive instars, and, thereby, constitute metamorphoses.

By analogy with developmental patterns among modern marine arthropod taxa, metamorphoses during early trilobite ontogeny correspond to radical modifications in life mode and ecology. Adult‐like trilobite protaspides possess a dorso‐ventrally flattened tergum which displays a coarsely featured prosopon and surface‐parallel spines; these are interpreted as benthic larvae. In contrast, nonadult‐like protaspid larvae display an ovoid to spheroidal shape with spine pairs that project at right angles to one another; these are considered to have been planktonic. Protaspid morphologies are compared and discussed in light of these inferred modes of life.     

Relationship between freshwater gastropods and plant communities reflecting various trophic levels

Plant communities were examined in ponds in Brittany (north-west France) and then classified into six types reflecting different trophic levels: oligotrophic, oligodystrophic, mesotrophic, meso-dystrophic, meso-eutrophic an eutrophic. In 45 of these ponds, aquatic snails were sampled in order to determine the relationship between the gastropod species richness and the water trophic levels as indicated by plant community types. The second aim of this study was to determine whether some gastropod species were characteristic of a particular trophic level. The number of plant communities in the ponds was also taken into consideration.A trophic gradient was found along the F1 axis on the principal plane of the correspondence analyses. The species richnesses low or zero and especially the lymneid, Lymnaea glabra were close to the oligo-dystrophic and oligotrophic communities. In contrast, the highest numbers of snail species (5 and above) were found in the most eutrophic ponds where Hippeutis complanatus, Planorbis planorbis, Lymnaea stagnalis and Planorbarius corneus were particularly common. The latter species inhabited the ponds including on average the greatest number of macrophyte communities but no significant differences were found between snail species. The ponds which contained the greatest numbers of plant communities included the richest gastropod communities (7 and more) but also the poorest ones (0 or 1 species). Relationships between freshwater snails, macrophytes and trophic levels are discussed.Laboratoire de Zoologie et d'Ecophysiologie     

Life history,ecology and longevity in bats

The evolutionary theory of aging predicts that life span should decrease in response to the amount of mortality caused by extrinsic sources. Using this prediction, we selected six life history and ecological factors to use in a comparative analysis of longevity among 64 bat species. On average, the maximum recorded life span of a bat is 3.5 times greater than a non-flying placental mammal of similar size. Records of individuals surviving more than 30 years in the wild now exist for five species. Univariate and multivariate analyses of species data, as well as of phylogenetically independent contrasts obtained using a supertree of Chiroptera, reveal that bat life span significantly increases with hibernation, body mass and occasional cave use, but decreases with reproductive rate and is not influenced by diet, colony size or the source of the record. These results are largely consistent with extrinsic mortality risk acting as a determinant of bat longevity. Nevertheless, the strong association between life span and both reproductive rate and hibernation also suggests that bat longevity is strongly influenced by seasonal allocation of non-renewable resources to reproduction. We speculate that hibernation may provide a natural example of caloric restriction, which is known to increase longevity in other mammals.     

Phenotypic plasticity of six unusual cercariae in nassariid gastropods and their relationships to the Acanthocolpidae and Brachycladiidae (Digenea)

Species-level relationships of a complex of six putative acanthocolpid cercariae with ventral keels from nassariid gastropods from Capricornia, Queensland (Cercaria capricornia I–VI) were explored using mitochondrial and nuclear DNA sequence data. Analysis of the large subunit of nuclear ribosomal DNA (rDNA), the internal transcribed spacer 2 rDNA and subunit 3 of the nicotinamide-adenine-dinucleotide dehydrogenase mitochondrial gene indicates that the six distinct morphotypes previously identified relate to only three discrete genotypes. Consequently, the six cercarial morphotypes that were inferred to represent six species and distinguished previously based on morphology and behaviour, are considered here to be comprised of three species (i.e. Cercaria capricornia I and II are considered the same species, C. capricornia types III to V are considered to belong to a second species and C. capricornia VI is considered to comprise the third species in this complex). This recognition of reduced diversity following molecular analysis runs contrary to the more frequently reported uncovering of cryptic diversity, especially when larval trematodes are examined. Phylogenetic analysis of these morphologically unusual cercariae supports their inclusion in the Acanthocolpidae. Bayesian inference analysis identifies three distinct clades: (a) Stephanostomum + Monostephanostomum; (b) the Brachycladiidae and Pleorchis; and (c) Tormopsolus and the present cercariae. Genus-level identification of these cercariae remains uncertain given the current lack of available comparative genetic data on nucleic acid databases.     

The L-isoaspartyl-O-methyltransferase in Caenorhabditis elegans larval longevity and autophagy

The protein L-isoaspartyl-O-methyltransferase, coded by the pcm-1 gene in Caenorhabditis elegans, participates in the repair of age-damaged proteins. We tested the ability of pcm-1-deficient nematodes to survive starvation stress as developmentally-arrested L1 larvae. We found that pcm-1 mutant L1 larvae do not survive as well as wild-type L1 larvae when incubated in M9 medium without nutrients. We then tested whether the starved L1 larvae could continue development when allowed access to food in a recovery assay. A loss of recovery ability with age was observed for all larvae, with little or no difference between the pcm-1 mutant and wild-type N2 larvae. Interestingly, when L1 larvae were starved in cholesterol-containing S medium or M9 medium supplemented with cholesterol, the survival rates of both mutant and wild-type animals nearly doubles, with pcm-1 larvae again faring more poorly than N2 larvae. Furthermore, L1 larvae cultured in these cholesterol-containing media show an increase in Sudan Black staining over animals cultured in M9 medium. The longevity defects of pcm-1 mutants previously seen in dauer larvae and here in L1 larvae suggest a defect in the ability of pcm-1 mutants to recycle and reuse old cellular components in pathways such as autophagy. Using an autophagosomal marker, we found evidence suggesting that the pcm-1 mutation may inhibit autophagy during dauer formation, suggesting that the absence of protein repair may also interfere with protein degradation pathways.     

Relationship between seed bank expression, adult longevity and aridity in species of Chaetanthera (Asteraceae) in central Chile

BACKGROUND AND AIMS: Broad surveys have detected inverse relationships between seed and adult longevity and between seed size and adult longevity. However, low and unpredictable precipitation is also associated with seed bank (SB) expression in semi-arid and arid areas. The relationship between adult longevity, SB formation, seed mass and aridity is examined in annual and perennial herbs of Chaetanthera (Asteraceae) from the Chilean Mediterranean-type climate and winter-rainfall desert areas over a precipitation range of one order of magnitude. METHODS: Seeds of 18 species and subtaxa (32 populations) were buried in field locations, and exhumed after two successive germination periods. Seeds not germinating in the field were tested in a growth chamber, and remnant intact seed tested for viability. Seed banks were classed as transient or persistent. The effect of life form, species, population and burial time on persistent SB size was assessed with factorial ANOVA. Persistent seed bank size was compared with the Martonne aridity index (shown to be a surrogate for inter-annual variation in precipitation) and seed size using linear regression. ANCOVA assessed the effect of life-form on SB size with aridity as covariate. KEY RESULTS: Three species had a transient SB and 15 a persistent SB. ANOVA revealed a significant effect of life-form on SB size with annuals having larger SB size and greater capacity to form a persistent SB than perennials. Significant inter-population variation in SB size was found in 64% of cases. Seed mass was negatively correlated with persistent SB size. Persistent seed bank size was significantly correlated with the Martonne aridity index in the perennial and annual species, with species from more arid areas having larger persistent SBs. However, when aridity was considered as a covariate, ANCOVA revealed no significant differences between the annual and perennial herbs. CONCLUSIONS: Persistent seed bank size in Chaetanthera appears to reflect environmental selection rather than any trade-off with adult longevity.     

Larval ecology of prosobranch gastropods and its bearing on biogeography and paleontology

The larval ecology of prosobranch gastropods, which ranges from long pelagic plankto-trophic life histories to directly developing lecithotrophic ones, has a strong influence on larval dispersion. Because of low migrative ability in the post-larval stage, gastropod distribution must depend fundamentally on larval dispersion. It is probable that the modes of larval dispersion relate importantly to the mechanism by which prosobranch populations become isolated, and consequently to their modes of speciation. This idea is applicable for analysis of fossil material, for both biological and oceanographical information.     

Rapid declines in metabolism explain extended coral larval longevity

Lecithotrophic, or non-feeding, marine invertebrate larvae generally have shorter pelagic larval durations (PLDs) than planktotrophic larvae. However, non-feeding larvae of scleractinian corals have PLDs far exceeding those of feeding larvae of other organisms and predictions of PLD based on energy reserves and metabolic rates, raising questions about how such longevity is achieved. Here, we measured temporal changes in metabolic rates and total lipid content of non-feeding larvae of four species of reef corals to determine whether changes in energy utilization through time contribute to extended larval durations. The temporal dynamics of both metabolic rates and lipid content were highly consistent among species. Prior to fertilization, metabolic rates were low (2.73–8.63 nmol O₂ larva^?1 h^?1) before rapidly increasing to a peak during embryogenesis and early development 1–2 days after spawning. Metabolic rates remained high until shortly after larvae first became competent to metamorphose and then declined by up to two orders of magnitude to levels at or below rates seen in unfertilized eggs over the following week. Larvae remained in this state of low metabolic activity for up to 2 months. Consistent with temporal patterns in metabolic rates, depletion of lipids was extremely rapid during early development and then slowed dramatically from 1 week onward. Despite the very low metabolic rates in these species, larvae continued to swim and retained competence for at least 2 months. The capacity of non-feeding coral larvae to enter a state of low metabolism soon after becoming competent to metamorphose significantly extends dispersal potential, thereby accruing advantages typically associated with planktotrophy, notably enhanced population connectivity.     

Relationship between adult and larval host plant selection and larval performance in the generalist moth, Trichoplusia ni

Adult oviposition preferences are expected to correlate with host plant suitability for the development of their offspring. For most lepidopteran species, this is particularly important as the hatching neonate larvae of many species are relatively immobile. Thus, the site of oviposition chosen by a female adult can greatly influence the probability of survival for her offspring. In the present study, we investigated the oviposition preference of adult Trichoplusia ni moths for six plant species to determine whether they could accurately rank the suitability of the plants for larval development. We also compared oviposition preferences to neonate larval acceptance and preference to determine whether the adult host range matched that of larval diet breath. Our results indicate that in two-choice and no-choice tests adult T. ni were able to rank the plants accurately, with the exception of anise hyssop. However, when given a choice of all six plants together, they laid more eggs on a plant that was not suitable for larval survival. Larvae accepted and fed on all plants in no-choice tests, and accurately ranked them according to larval performance. We conclude that neonate larvae are better able than adults to rank plants according to larval performance, and that larval diet breadth is wider than the range of plants accepted by adults. We also provide a discussion of the reduced accuracy of adult oviposition preference with increased plant choices.     

The foraging ecology of larval and juvenile fishes

Knowledge of the foraging ecology of fishes is fundamental both to understanding the processes that function at the individual, population and community levels, and for the management and conservation of their populations and habitats. Furthermore, the factors that influence the acquisition and assimilation of food can have significant consequences for the condition, growth, survival and recruitment of fishes. The majority of marine and freshwater fish species are planktivorous at the onset of exogenous nutrition and have a limited ability to detect, capture, ingest and digest prey. Improvements in vision, development of fins and associated improvements in swimming performance, increases in gape size and development of the alimentary tract during ontogeny often lead to shifts in diet composition. Prey size, morphology, behaviour and abundance can all influence the prey selection of larval and juvenile fishes. Differences in feeding behaviour between fish species, individuals or during ontogeny can also be important, as can inter- and intraspecific interactions (competition, predation risk). Temporal (diel, seasonal, annual) and spatial (microhabitat, mesohabitat, macrohabitat, regional) variations in prey availability can have important implications for the prey selection, diet composition, growth, survival, condition and, ultimately, recruitment success of fishes. For fish populations to persist, habitat must be available in sufficient quality and quantity for the range of activities undertaken during all periods of development. Habitats that enhance the diversity, size ranges and abundance of zooplankton should ensure that sufficient food resources are available to larval and juvenile fishes.     

Complete lack of mitochondrial divergence between two species of NE Atlantic marine intertidal gastropods

Some mitochondrial introgression is common between closely related species, but distinct species rarely show substantial introgression in their entire distribution range. In this study, however, we report a complete lack of mitochondrial divergence between two sympatric species of flat periwinkles (Littorina fabalis and Littorina obtusata) which, based on previous allozyme studies, diverged approximately 1 Ma. We re‐examined their species status using both morphology (morphometric analysis) and neutral genetic markers (microsatellites) and our results confirmed that these species are well separated. Despite this, the two species shared all common cytochrome‐b haplotypes throughout their NE Atlantic distribution and no deep split between typical L. fabalis and L. obtusata haplotypes could be found. We suggest that incomplete lineage sorting explains most of the lack of mitochondrial divergence between these species. However, coalescent‐based analyses and the sympatric sharing of unique haplotypes suggest that introgressive hybridization also has occurred.     

Host longevity and parasite species richness in mammals

Hosts and parasites co-evolve, with each lineage exerting selective pressures on the other. Thus, parasites may influence host life-history characteristics, such as longevity, and simultaneously host life-history may influence parasite diversity. If parasite burden causes increased mortality, we expect a negative association between host longevity and parasite species richness. Alternatively, if long-lived species represent a more stable environment for parasite establishment, host longevity and parasite species richness may show a positive association. We tested these two opposing predictions in carnivores, primates and terrestrial ungulates using phylogenetic comparative methods and controlling for the potentially confounding effects of sampling effort and body mass. We also tested whether increased host longevity is associated with increased immunity, using white blood cell counts as a proxy for immune investment. Our analyses revealed weak relationships between parasite species richness and longevity. We found a significant negative relationship between longevity and parasite species richness for ungulates, but no significant associations in carnivores or primates. We also found no evidence for a relationship between immune investment and host longevity in any of our three groups. Our results suggest that greater parasite burden is linked to higher host mortality in ungulates. Thus, shorter-lived ungulates may be more vulnerable to disease outbreaks, which has implications for ungulate conservation, and may be applicable to other short-lived mammals.     

Connecting species richness, abundance and body size in deep-sea gastropods

Aim This paper examines species richness, abundance, and body size in deep‐sea gastropods and how they vary over depth, which is a strong correlate of nutrient input. Previous studies have documented the empirical relationships among these properties in terrestrial and coastal ecosystems, but a full understanding of how these patterns arise has yet to be obtained. Examining the relationships among macroecological variables is a logical progression in deep‐sea ecology, where patterns of body size, diversity, and abundance have been quantified separately but not linked together. Location 196–5042 m depth in the western North Atlantic. Method Individuals analysed represent all Vetigastropoda and Caenogastropoda (Class Gastropoda) with intact shells, excluding Ptenoglossa, collected by the Woods Hole Benthic Sampling Program (3424 individuals representing 80 species). Biovolume was measured for every individual separately (i.e. allowing the same species to occupy multiple size classes) and divided into log₂ body size bins. Analyses were conducted for all gastropods together and separated into orders and depth regions (representing different nutrient inputs). A kernel smoothing technique, Kolmogorov‐Smirnov test of fit, and OLS and RMA were used to characterize the patterns. Results Overall, the relationship between the number of individuals and species is right skewed. There is also a positive linear relationship between the number of individuals and the number of species, which is independent of body size. Variation among these relationships is seen among the three depth regions. At depths inferred to correspond with intermediate nutrient input levels, species are accumulated faster given the number of individuals and shift from a right‐skewed to a log‐normal distribution. Conclusion A strong link between body size, abundance, and species richness appears to be ubiquitous over a variety of taxa and environments, including the deep sea. However, the nature of these relationships is affected by the productivity regime and scale at which they are examined.     

A first glimpse of larval ecology of halibut species in the Gulf of St. Lawrence,Canada

Knowledge of the larval ecology of winter-spawning fish from the Estuary and Gulf of St. Lawrence, Canada, remains scarce due to the seasonal ice cover that prevents ichthyoplankton sampling using conventional methods. Two winter-spawning species, Atlantic halibut (AH, Hippoglossus hippoglossus) and Greenland halibut (GH, Reinhardtius hippoglossoides), support the most important groundfish fisheries of this area. In March 2020, the authors captured 10 halibut larvae ranging in size from 5 to 14 mm during an opportunistic survey in the GSL onboard an icebreaking vessel. Of these, eight were AH and two GH. Judging by their very small size, the larvae were only a few days old, suggesting that the spawning grounds are close to the capture sites. This effort constitutes a first step in validating the putative spawning areas for these two important GSL stocks. This knowledge is important for the conservation and sustainable management of these fisheries.     

Ontogenetic torsion in two basal gastropods occurs without shell attachments for larval retractor muscles

Results of this study on two species of vetigastropods contradict the long-standing hypothesis, originally proposed by Garstang (1929), that the larval retractor muscles power the morphogenetic movement of ontogenetic torsion in all basal gastropods. In the trochid Calliostoma ligatum and the keyhole limpet Diodora aspera, the main and accessory larval retractor muscles failed to establish attachments onto the protoconch (larval shell) when the antibiotics streptomycin sulfate and penicillin G were added to cultures soon after fertilization. Defects in protoconch mineralization were also observed. Despite these abnormalities, developing larvae of these species accomplished complete or almost complete ontogenetic torsion, a process in which the head and foot rotate by 180 degrees relative to the protoconch and visceral mass. Analysis by using phalloidin-fluorophore conjugate and transmission electron microscopy showed that myofilaments differentiated within myocytes of the larval retractor muscles and adherens-like junctions formed between muscle and mantle epithelial cells in both normal and abnormal larvae. However, in abnormal larvae, apical microvilli of mantle cells that were connected to the base of the larval retractor muscles failed to associate with an extracellular matrix that normally anchors the microvilli to the mineralized protoconch. If morphogenesis among extant, basal gastropods preserves the original developmental alteration that created gastropod torsion, as proposed by Garstang (1929), then the alteration involved something other than the larval retractor muscles. Alternatively, the developmental process of torsion has evolved subsequent to its origin in at least some basal gastropod clades so that the original alteration is no longer preserved in these clades.