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"Gastropoda - physiology"
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The Central Paratethys Sea—rise and demise of a Miocene European marine biodiversity hotspot
The Miocene Climate Optimum (MCO, ~ 17–14 Ma) was a time of extraordinary marine biodiversity in the Circum-Mediterranean Region. This boom is best recorded in the deposits of the vanished Central Paratethys Sea, which covered large parts of central to southeastern Europe. This sea harbored an extraordinary tropical to subtropical biotic diversity. Here, we present a georeferenced dataset of 859 gastropod species and discuss geodynamics and climate as the main drivers to explain the changes in diversity. The tectonic reorganization around the Early/Middle Miocene boundary resulted in the formation of an archipelago-like landscape and favorable conditions of the MCO allowed the establishment of coral reefs. Both factors increased habitat heterogeneity, which boosted species richness. The subsequent cooling during the Middle Miocene Climate Transition (~ 14–13 Ma) caused a drastic decline in biodiversity of about 67%. Among the most severely hit groups were corallivorous gastropods, reflecting the loss of coral reefs. Deep-water faunas experienced a loss by 57% of the species due to changing patterns in circulation. The low sea level led to a biogeographic fragmentation reflected in higher turnover rates. The largest turnover occurred with the onset of the Sarmatian when bottom water dysoxia eradicated the deep-water fauna whilst surface waters-dwelling planktotrophic species underwent a crisis.
Journal Article
The Scaly-foot Snail genome and implications for the origins of biomineralised armour
The Scaly-foot Snail,
Chrysomallon squamiferum
, presents a combination of biomineralised features, reminiscent of enigmatic early fossil taxa with complex shells and sclerites such as sachtids, but in a recently-diverged living species which even has iron-infused hard parts. Thus the Scaly-foot Snail is an ideal model to study the genomic mechanisms underlying the evolutionary diversification of biomineralised armour. Here, we present a high-quality whole-genome assembly and tissue-specific transcriptomic data, and show that scale and shell formation in the Scaly-foot Snail employ independent subsets of 25 highly-expressed transcription factors. Comparisons with other lophotrochozoan genomes imply that this biomineralisation toolkit is ancient, though expression patterns differ across major lineages. We suggest that the ability of lophotrochozoan lineages to generate a wide range of hard parts, exemplified by the remarkable morphological disparity in Mollusca, draws on a capacity for dynamic modification of the expression and positioning of toolkit elements across the genome.
The Scaly-foot Snail,
Chrysomallon squamiferum
, is a model for understanding the evolution of biomineralised armour. Here, the authors present a chromosome-level reference genome assembly and tissue-specific transcriptomic data for this enigmatic organism.
Journal Article
Body-size evolution in gastropods across the Plio-Pleistocene extinction in the western Atlantic
The Plio-Pleistocene turnover event in the western Atlantic following the closure of the Central American Seaway involved high rates of extinction for both gastropod and bivalve molluscs. This extinction was associated with declining nutrient conditions and has been presumed to be associated with a decrease in molluscan body size. Previous work which has been concordant with this expectation, however, has either focused on bivalves or not considered the effects of the recovery post extinction. In three phylogenetically diverse clades, we found that body-size evolution in gastropods across the turnover event is likely tied to ecology. One clade increased in size, one decreased, and another exhibited no substantial change. Individual species lineages exhibit a mixture of microevolutionary changes from the Pliocene to today. This study indicates that gastropod body-size evolution may be more complex than in bivalves, with ecology and other functional traits playing a significant role. Macroevolutionary processes, especially whether a clade re-radiated post extinction, were found to be important. Indeed, a low portion of extant diversity consists of survivors from clades that increased in size or have similar size distributions among their species relative to the Pliocene.
Journal Article
The origin and diversification of pteropods precede past perturbations in the Earth’s carbon cycle
Pteropods are a group of planktonic gastropods that are widely regarded as biological indicators for assessing the impacts of ocean acidification. Their aragonitic shells are highly sensitive to acute changes in ocean chemistry. However, to gain insight into their potential to adapt to current climate change, we need to accurately reconstruct their evolutionary history and assess their responses to past changes in the Earth’s carbon cycle. Here, we resolve the phylogeny and timing of pteropod evolution with a phylogenomic dataset (2,654 genes) incorporating new data for 21 pteropod species and revised fossil evidence. In agreement with traditional taxonomy, we recovered molecular support for a division between “sea butterflies” (Thecosomata; mucus-web feeders) and “sea angels” (Gymnosomata; active predators). Molecular dating demonstrated that these two lineages diverged in the early Cretaceous, and that all main pteropod clades, including shelled, partially-shelled, and unshelled groups, diverged in the mid- to late Cretaceous. Hence, these clades originated prior to and subsequently survived major global change events, including the Paleocene–Eocene Thermal Maximum (PETM), the closest analog to modern-day ocean acidification and warming. Our findings indicate that planktonic aragonitic calcifiers have shown resilience to perturbations in the Earth’s carbon cycle over evolutionary timescales.
Journal Article
Widespread shifts in the coastal biota of northern California during the 2014–2016 marine heatwaves
During 2014–2016, severe marine heatwaves in the northeast Pacific triggered well-documented disturbances including mass mortalities, harmful algal blooms, and declines in subtidal kelp beds. However, less attention has been directed towards understanding how changes in sea surface temperature (SST) and alongshore currents during this period influenced the geographic distribution of coastal taxa. Here, we examine these effects in northern California, USA, with a focus on the region between Point Reyes and Point Arena. This region represents an important biogeographic transition zone that lies <150 km north of Monterey Bay, California, where numerous southern species have historically reached their northern (poleward) range limits. We report substantial changes in geographic distributions and/or abundances across a diverse suite of 67 southern species, including an unprecedented number of poleward range extensions (37) and striking increases in the recruitment of owl limpets (
Lottia gigantea
) and volcano barnacles (
Tetraclita rubescens
). These ecological responses likely arose through the combined effects of extreme SST, periods of anomalous poleward flow, and the unusually long duration of heatwave events. Prolonged marine heatwaves and enhanced poleward dispersal may play an important role in longer-term shifts in the composition of coastal communities in northern California and other biogeographic transition zones.
Journal Article
Species Selection Favors Dispersive Life Histories in Sea Slugs, but Higher Per-Offspring Investment Drives Shifts to Short-Lived Larvae
For 40 years, paleontological studies of marine gastropods have suggested that species selection favors lineages with short-lived (lecithotrophic) larvae, which are less dispersive than long-lived (planktotrophic) larvae. Although lecithotrophs appeared to speciate more often and accumulate over time in some groups, lecithotrophy also increased extinction rates, and tests for state-dependent diversification were never performed. Molecular phylogenies of diverse groups instead suggested lecithotrophs accumulate without diversifying due to frequent, unidirectional character change. Although lecithotrophy has repeatedly originated in most phyla, no adult trait has been correlated with shifts in larval type. Thus, both the evolutionary origins of lecithotrophy and its consequences for patterns of species richness remain poorly understood. Here, we test hypothesized links between development mode and evolutionary rates using likelihood-based methods and a phylogeny of 202 species of gastropod molluscs in Sacoglossa, a clade of herbivorous sea slugs. Evolutionary quantitative genetics modeling and stochastic character mapping supported 27 origins of lecithotrophy. Tests for correlated evolution revealed lecithotrophy evolved more often in lineages investing in extra-embryonic yolk, the first adult trait associated with shifts in development mode across a group. However, contrary to predictions from paleontological studies, species selection actually favored planktotrophy; most extant lecithotrophs originated through recent character change, and did not subsequently diversify. Increased offspring provisioning in planktotrophs thus favored shifts to short-lived larvae, which led to short-lived lineages over macroevolutionary time scales. These findings challenge long-standing assumptions about the effects of alternative life histories in the sea. Species selection can explain the long-term persistence of planktotrophy, the ancestral state in most clades, despite frequent transitions to lecithotrophy.
Journal Article
Evolved differences in energy metabolism and growth dictate the impacts of ocean acidification on abalone aquaculture
Ocean acidification (OA) poses a major threat to marine ecosystems and shellfish aquaculture. A promising mitigation strategy is the identification and breeding of shellfish varieties exhibiting resilience to acidification stress. We experimentally compared the effects of OA on two populations of red abalone (Haliotis rufescens), a marine mollusc important to fisheries and global aquaculture. Results from our experiments simulating captive aquaculture conditions demonstrated that abalone sourced from a strong upwelling region were tolerant of ongoing OA, whereas a captiveraised population sourced from a region of weaker upwelling exhibited significant mortality and vulnerability to OA. This difference was linked to population-specific variation in the maternal provisioning of lipids to offspring, with a positive correlation between lipid concentrations and survival under OA. This relationship also persisted in experiments on second-generation animals, and larval lipid consumption rates varied among paternal crosses, which is consistent with the presence of genetic variation for physiological traits relevant for OA survival. Across experimental trials, growth rates differed among family lineages, and the highest mortality under OA occurred in the fastest growing crosses. Identifying traits that convey resilience to OA is critical to the continued success of abalone and other shellfish production, and these mitigation efforts should be incorporated into breeding programs for commercial and restoration aquaculture.
Journal Article
Wheel running in the wild
The importance of exercise for health and neurogenesis is becoming increasingly clear. Wheel running is often used in the laboratory for triggering enhanced activity levels, despite the common objection that this behaviour is an artefact of captivity and merely signifies neurosis or stereotypy. If wheel running is indeed caused by captive housing, wild mice are not expected to use a running wheel in nature. This however, to our knowledge, has never been tested. Here, we show that when running wheels are placed in nature, they are frequently used by wild mice, also when no extrinsic reward is provided. Bout lengths of running wheel behaviour in the wild match those for captive mice. This finding falsifies one criterion for stereotypic behaviour, and suggests that running wheel activity is an elective behaviour. In a time when lifestyle in general and lack of exercise in particular are a major cause of disease in the modern world, research into physical activity is of utmost importance. Our findings may help alleviate the main concern regarding the use of running wheels in research on exercise.
Journal Article
SlugAtlas, a histological and 3D online resource of the land slugs Deroceras laeve and Ambigolimax valentianus
Due to their distinctive anatomical characteristics, land slugs are appealing research subjects from a variety of angles, including stem cell biology, regeneration, embryonic development, allometry, and neurophysiology. Here we present SlugAtlas, an anatomical and histological online resource of the land slugs Deroceras laeve and Ambigolimax valentianus . The atlas is composed of series of histological sections on the horizontal, sagittal, and transversal planes for both species with 3D viewing tools of their major organs. The atlas was used in this work for a comparative analysis of the major organs and tissues of these two species. We provide a comprehensive histological description of them and an explanation of novel findings of unique features of their anatomy. For D . laeve , we additionally studied its ability for degrowth and regrowth, a feature that characterizes animals with high regeneration potential and obtained initial results on the study of the regeneration of its tail. SlugAtlas is a resource that is also built to accommodate future growth and, along with the experimental techniques that we have developed, will provide the foundation for research projects in a variety of biological domains.
Journal Article