Shell-based genus-level reclassification of the Family Vasidae (Mollusca: Neogastropoda).

The neogastropod family Vasidae comprises a small group of Late Eocene to Recent neogastropods with large, often ornate shells. A new, shell-based morphological classification of the family is proposed, in which ten genera are recognized: Altivasum Hedley, 1914, Aristovasum gen. nov. (type species: Turbinella cassiforme Kiener, 1840), Florivasum gen. nov. (type species: Turbinella tubifera Anton, 1838), Globivasum Abbott, 1950 (type species: Turbinella nuttingi Henderson, 1919, but expanded here), Hystrivasum Olsson & Petit, 1964 (type species: Vasum horridum Heilprin, 1887), Rhinovasum gen. nov. (type species: Voluta rhinoceros Gmelin, 1791), Siphovasum Rehder & Abbott, 1951, Tudivasum Rosenberg & Petit, 1987, Vasum Rding, 1798 (here restricted to a reef-associated group of three species typified by Murex turbinellus Linnaeus, 1758), and Volutella Perry, 1810 (here resurrected from synonymy with Vasum, type species Voluta muricata Born, 1778). Biogeographically the Vasidae exhibit a deep divergence between the Atlantic-East Pacific and Indo-West Pacific realms dating to the Early Miocene.

The illusion of balance in the history of the biosphere.

Earth's surface has been irreversibly altered by the activity of organisms, a process that has accelerated as the power of the biosphere (the rate at which life extracts and deploys energy) has increased over time. This trend is incompatible with the expectation that the inputs to Earth's surface of life's materials from the crust and mantle be matched by export from Earth's surface to long-term reservoirs. Here, I suggest that the collective activity of organisms has always violated this balance. The biosphere's ability to extract, retain, recycle, and accumulate materials has allowed living biomass to increase and for exports to decrease over very long timescales. This collective metabolism implies a net transfer of materials from the planet's interior to its surface. The combination of metabolic innovations, competition, adaptive evolution, and the establishment of collaborative economic feedback in ecosystems created dynamic ecological stability despite great spatial and temporal heterogeneity in physical and biological inputs and export of nutrients into and out of the biosphere. Models of geochemical cycling must take the fundamental role of living organisms and the evolutionary changes in these roles into account to explain past and future conditions.

When does natural selection take place?

Although many studies of form and function find a correlation between performance and adaptive specialization, others fail to discern such a tight link despite careful monitoring and observation. This inconsistency among studies raises the question of when, how often, and how effectively natural selection and the organism's own activities operate to maintain or improve the adapted state. I suggest here that most organisms operate well within the limits of their capacities (safety factors) most of the time and that interactions and circumstances that cause natural selection and test the body's limits come in discrete, intermittent events rather than as continuously present or chronic conditions. Everyday life without such events does not test performance limits and therefore does not usually result in natural selection. This perspective on selection as rare, intermittent testing by ecological agencies suggests that studies of selective processes and activity in the wild should focus on observing and measuring the intensity and frequency of selective events and responses, intense challenges stemming from agencies such as predators, competitors, mating-related rituals, and extreme weather.

Deep resilience: An evolutionary perspective on calcification in an age of ocean acidification.

The success of today's calcifying organisms in tomorrow's oceans depends, in part, on the resilience of their skeletons to ocean acidification. To the extent this statement is true there is reason to have hope. Many marine calcifiers demonstrate resilience when exposed to environments that mimic near-term ocean acidification. The fossil record similarly suggests that resilience in skeletons has increased dramatically over geologic time. This "deep resilience" is seen in the long-term stability of skeletal chemistry, as well as a decreasing correlation between skeletal mineralogy and extinction risk over time. Such resilience over geologic timescales is often attributed to genetic canalization-the hardening of genetic pathways due to the evolution of increasingly complex regulatory systems. But paradoxically, our current knowledge on biomineralization genetics suggests an opposing trend, where genes are co-opted and shuffled at an evolutionarily rapid pace. In this paper we consider two possible mechanisms driving deep resilience in skeletons that fall outside of genetic canalization: microbial co-regulation and macroevolutionary trends in skeleton structure. The mechanisms driving deep resilience should be considered when creating risk assessments for marine organisms facing ocean acidification and provide a wealth of research avenues to explore.

Imbricated shell sculpture in benthic bivalves.

Molluscan shells display a high diversity of external sculpture. Sculptural elements may be symmetrical, where both edges of an element are morphologically similar, or asymmetrical, where one edge is steeper than the other. Asymmetrical sculpture can be ratcheted, with the leading edges (those in the direction of locomotion or growth) less steep than the trailing edges, or imbricated (leading edges steeper than trailing edges). While the ratcheted sculpture is better known, the diversity of imbricated sculpture has remained largely unexplored. In a survey of extant benthic shell-bearing molluscs, we document imbricated sculpture primarily in epifaunal bivalves or on the exposed sectors of shells of semi-infaunal bivalves. Imbricated sculpture is particularly widespread in pteriomorphian bivalves, but it is absent in the subclade Mytiloidea as well as in highly mobile Pectinidae. It also occurs in many carditid bivalves (Archiheterodonta) and in phylogenetically scattered euheterodonts. In several infaunal bivalves including species of Cardites (Carditidae), Hecuba (Donacidae), and Chione (Veneridae), comarginal elements on the posterior sector are imbricated whereas anterior comarginal ridges are ratcheted. Imbricated sculpture in bivalves tends to be concentrated on the upper (left) valves of pectinids or on the posterior sector of both valves in archiheterodonts and euheterodonts. Imbricated sculpture is uncommon in gastropods, even in epifaunal species, but does occur in the collabral ridges in some Vasidae and a few other groups. Expression of imbricated sculpture does not depend on shell mineral composition or microstructure. The ecological distribution and within-shell pattern of expression of imbricated sculpture point to the likelihood that this type of asymmetrical sculpture is both widespread and potentially functional. Additionally, we present a potential methodology whereby shell sculpture categories (symmetrical, ratcheted, and imbricated) may be quantified by comparing the lengths of corresponding leading and trailing edges across the shell surface.

Evolutionary norm-breaking and extinction in the marine tropics.

Evolutionary innovations, defined as character states that transcend clade norms, are often studied in an exclusively phylogenetic context, but their distribution in time and space indicates that geography also influences the evolution of new ecological, morphological, and physiological traits. In an analysis of 99 fossillzable, norm-breaking innovations in tropical marine Neogene molluscan clades that arose uniquely in either (but not in both) the Indo-West Pacific (IWP) or Atlantic-East Pacific (AEP) realms, I show that there are far more innovations in the IWP (79%) than those in the AEP (21%). Most of the innovations are interpretable as defensive or competitive adaptations or as indicators of extreme habitat specialization. Although the innovations arose in taxonomically rich biotas, only 9% are associated with subclades comprising 10 or more species each, indicating that they contributed little to overall taxonomic richness. Compilations of extant species in 30 pantropical molluscan clades show that the IWP accounts for 71% of tropical shallow-water species, implying that the per-species incidence of norm-breaking innovations is higher there than in the AEP. Only 5% of innovations became extinct in the IWP as compared with 38% in the AEP, mirroring a similar difference in the magnitudes of Late Miocene and later taxonomic extinction in the two realms. These data imply that large-scale disruption strongly limits norm-breaking innovation. Opportunities for adaptive innovation are therefore likely to be few in today's heavily overexploited and disturbed biosphere.

Short-term paleogeographic reorganizations and climate events shaped diversification of North American freshwater gastropods over deep time.

What controls species diversity and diversification is one of the major questions in evolutionary biology and paleontology. Previous studies have addressed this issue based on various plant and animal groups, geographic regions, and time intervals. However, as most previous research focused on terrestrial or marine ecosystems, our understanding of the controls on diversification of biota (and particularly invertebrates) in freshwater environments in deep time is still limited. Here, we infer diversification rates of North American freshwater gastropods from the Late Triassic to the Pleistocene and explore potential links between shifts in speciation and extinction and major changes in paleogeography, climate, and biotic interactions. We found that variation in the speciation rate is best explained by changes in continental fragmentation, with rate shifts coinciding with major paleogeographic reorganizations in the Mesozoic, in particular the retreat of the Sundance Sea and subsequent development of the Bighorn wetland and the advance of the Western Interior Seaway. Climatic events in the Cenozoic (Middle Eocene Climate Optimum, Miocene Climate Optimum) variably coincide with shifts in speciation and extinction as well, but no significant long-term association could be detected. Similarly, no influence of diversity dependence was found across the entire time frame of ~ 214 Myr. Our results indicate that short-term climatic events and paleogeographic changes are relevant to the diversification of continental freshwater biota, while long-term trends have limited effect.

History's legacy: Why future progress in ecology demands a view of the past.

History has profoundly affected the composition, distribution, and abundances of species in contemporary ecosystems. A full understanding of how ecosystems work and change must therefore take history into account. We offer four well-studied examples illustrating how a knowledge of history has strengthened interpretations of modern systems: the development of molluscan antipredatory defenses in relation to shell-breaking predators; the North Pacific kelp ecosystem with sea otters, smaller predators, sea urchins, and large herbivores; estuarine ecosystems affected by the decline in oysters and other suspension feeders; and the legacy of extinct large herbivores and frugivores in tropical American forests. Many current ecological problems would greatly benefit from a historical perspective. We highlight four of these: soil depletion and tree stunting in forests related to the disappearance of large consumers; the spread of anoxic dead zones in the ocean, which we argue could be mitigated by restoring predator and suspension-feeding guilds; ocean acidification, which would be alleviated by more nutrient recycling by consumers in the aerobic ecosystem; and the relation between species diversity and keystone predators, a foundational concept that is complicated by simplified trophic relationships in modern ecosystems.

Are saltmarshes younger than mangrove swamps?

Temperate saltmarshes and tropical mangrove swamps (mangals) are marine-influenced, productive ecosystems that enhance nutrient transfers between land and sea and facilitate colonization of lineages between terrestrial and marine habitats. Mangals have existed since the late Cretaceous, but the time of origin of saltmarshes is less clear. On the basis of phylogenetic and fossil evidence for plants and molluscs specialized to these ecosystems, I propose that saltmarsh vegetation of angiosperms began during the latest Eocene to Early Oligocene (35-30 Ma), at least 34 m.y. after the origin of mangals. The plants that colonized saltmarshes then and later have mainly temperate origins, contrasting with the tropical-forest origins of mangroves. Unlike the plants, the few saltmarsh-specialized molluscs are derived from tropical lineages and reflect recent colonizations. The development of saltmarshes during the Neogene enhanced near shore productivity along temperate and Arctic coastlines.

Ecophysiological steps of marine adaptation in extant and extinct non-avian tetrapods.

Marine reptiles and mammals are phylogenetically so distant from each other that their marine adaptations are rarely compared directly. We reviewed ecophysiological features in extant non-avian marine tetrapods representing 31 marine colonizations to test whether there is a common pattern across higher taxonomic groups, such as mammals and reptiles. Marine adaptations in tetrapods can be roughly divided into aquatic and haline adaptations, each of which seems to follow a sequence of three steps. In combination, these six categories exhibit five steps of marine adaptation that apply across all clades except snakes: Step M1, incipient use of marine resources; Step M2, direct feeding in the saline sea; Step M3, water balance maintenance without terrestrial fresh water; Step M4, minimized terrestrial travel and loss of terrestrial feeding; and Step M5, loss of terrestrial thermoregulation and fur/plumage. Acquisition of viviparity is not included because there is no known case where viviparity evolved after a tetrapod lineage colonized the sea. A similar sequence is found in snakes but with the haline adaptation step (Step M3) lagging behind aquatic adaptation (haline adaptation is Step S5 in snakes), most likely because their unique method of water balance maintenance requires a supply of fresh water. The same constraint may limit the maximum body size of fully marine snakes. Steps M4 and M5 in all taxa except snakes are associated with skeletal adaptations that are mechanistically linked to relevant ecophysiological features, allowing assessment of marine adaptation steps in some fossil marine tetrapods. We identified four fossil clades containing members that reached Step M5 outside of stem whales, pinnipeds, sea cows and sea turtles, namely Eosauropterygia, Ichthyosauromorpha, Mosasauroidea, and Thalattosuchia, while five other clades reached Step M4: Saurosphargidae, Placodontia, Dinocephalosaurus, Desmostylia, and Odontochelys. Clades reaching Steps M4 and M5, both extant and extinct, appear to have higher species diversity than those only reaching Steps M1 to M3, while the total number of clades is higher for the earlier steps. This suggests that marine colonizers only diversified greatly after they minimized their use of terrestrial resources, with many lineages not reaching these advanced steps. Historical patterns suggest that a clade does not advance to Steps M4 and M5 unless these steps are reached early in the evolution of the clade. Intermediate forms before a clade reached Steps M4 and M5 tend to become extinct without leaving extant descendants or fossil evidence. This makes it difficult to reconstruct the evolutionary history of marine adaptation in many clades. Clades that reached Steps M4 and M5 tend to last longer than other marine tetrapod clades, sometimes for more than 100 million years.

Getting Out of Arms' Way: Star Wars and Snails on the Seashore.

AbstractMany shell-bearing gastropods exhibit pre-capture behaviors when encountering predatory asteroid sea stars. As shown in this meta-analysis of 48 studies on 24 sea star and 100 gastropod and chiton species, almost three-quarters of prey escape by moving or tumbling away, whereas the remaining species clamp tightly to the substratum or otherwise resist. The aim of the present paper is to correlate these behaviors with predicted shell traits, including those with gravitational stability for species that escape on the substratum and those that clamp, and those with a strongly sculptured shell in species that resist sea star attacks. Escaping species and those that clamp have gravitationally stable shells, with the center of gravity located above the broad aperture and large foot. Species that resist have significantly more sculptured shells. All of these traits would also work well in encounters with other slow-moving predators, such as gastropods and planarians. Although the sea stars are generalist predators, and the gastropods have many enemies besides sea stars, cool-water gastropods are well adapted to predatory sea stars on temperate and polar coasts, where most hard-bottom sea stars with molluscan diets occur. The prominence of escape among cool-water gastropods seems contradictory, given that locomotor speed rises with increasing temperature; but tropical gastropods rely more on armor than on escape, because of the prevalence of faster, more powerful predators in warm water. The black pigment of shells of many temperate prey species of sea stars might confer crypsis against these predators.

The ecology of marine colonization by terrestrial arthropods.

Terrestrial arthropods often colonized and became important in freshwater ecosystems, but did so less often and with little consequence in marine habitats. This pattern cannot be explained by the physical properties of water alone or by limitations of the terrestrial arthropod body plan alone. One hypothesis is that transitions among terrestrial, aquatic and marine ecosystems are unlikely when well-adapted incumbent species in the recipient realm collectively resist entry by initially less well adapted newcomers. I evaluated and modified this hypothesis by examining the properties of donor and recipient ecosystems and the roles that insects play or do not play in each. I argue that the insularity and diminished competitiveness of most freshwater ecosystems makes them vulnerable to invasion from land and sea, and largely prevent transitions from freshwater to terrestrial and marine habitats by arthropods. Small terrestrial arthropods emphasize high locomotor performance and long-distance communication, traits that work less well in the denser, more viscous medium of water. These limitations pose particular challenges for insects colonizing highly escalated marine ecosystems, where small incumbent species rely more on passive than on active defences. Predatory insects are less constrained than herbivores, wood-borers, filter-feeders, sediment burrowers and social species.

Why do chitons curl into a ball?

Many animals with external armour, such as hedgehogs, isopods and trilobites, curl into a protective ball when disturbed. However, in situations where predators would engulf an exposed animal whole, regardless of position, conglobation may provide limited added defence and the benefits were previously unclear. We show that polyplacophoran molluscs (chitons) are three times less likely to spend time curled into a ball in the presence of a predator. When the cue of a potential predator is present, animals instead spend significantly more time in active, high risk, high reward behaviours such as arching, balancing on the head and tail ends of their girdle and pushing the soft foot up into an exposed position. Arching increases vulnerability, but also can increase the likelihood of rapidly encountering new substratum that would allow the animal to right itself. In some other animals, the ability to roll into a ball is associated with rolling away from danger. Curling into a ball would improve mobility, to be rolled on to a safer position, but reattachment is the higher priority for chitons in the face of danger.

The efficiency paradox: How wasteful competitors forge thrifty ecosystems.

Organic waste, an inevitable byproduct of metabolism, increases in amount as metabolic rates (per capita power) of animals and plants rise. Most of it is recycled within aerobic ecosystems, but some is lost to the system and is sequestered in the crust for millions of years. Here, I identify and resolve a previously overlooked paradox concerning the long-term loss of organic matter. In this efficiency paradox, high-powered species are inefficient in that they release copious waste, but the ecosystems they inhabit lose almost no organic matter. Systems occupied by more efficient low-powered species suffer greater losses because of less efficient recycling. Over Phanerozoic time, ecosystems have become more productive and increasingly efficient at retaining and redistributing organic matter even as opportunistic and highly competitive producers and consumers gained power and became less efficient. These patterns and trends are driven by natural selection at the level of individuals and coherent groups, which favors winners that are more powerful, active, and wasteful. The activities of these competitors collectively create conditions that are increasingly conducive to more efficient recycling and retention of organic matter in the ecosystem.

Unidirectional grass hairs usher insects away from meristems.

Grasses are major agricultural products worldwide and they are critical to ecosystem function in many terrestrial habitats. Despite their global importance, we know relatively little about their defenses against herbivory. Grasses tend to be tolerant of leaf loss because their valuable meristems are located underground, out of reach for above ground herbivores. Many grasses have unidirectional leaf hairs, prickles, and spines that make moving up the leaf blade easy, but make moving down, toward the meristem, difficult. We tested the hypothesis that unidirectional grass hairs direct small arthropod herbivores away from the meristems. In a field survey of the distribution of herbivore damage, we found that leaf tips received five times more damage than leaf bases for Avena barbata. Early-instar grasshoppers fed three times as often on leaf tops as on leaf bases of pubescent individuals in a common garden laboratory experiment. This effect was not observed for glabrous individuals where grasshoppers damaged leaf bases as often as leaf tops. A common generalist caterpillar, Heliothus virescens, was more than twice as likely to turn in the direction of the hairs, away from the meristems, when it encountered pubescent leaves of A. barbata. However, larger caterpillars of the generalist feeder Arctia virginalis showed no directional bias when they encountered pubescent leaves. In common garden experiments, selection on pubescence was weak and inconsistent over space and time. Under some circumstances, individuals of A. barbata with pubescent leaves were more likely to produce seeds than were individuals with fewer hairs. The surveys, behavioral experiments with small insects, and estimates of lifetime reproduction all support the hypothesis that unidirectional leaf hairs on A. barbata, and perhaps other grasses, serve as an unstudied defense that direct small herbivores away from the meristems.

Comparative biogeography: innovations and the rise to dominance of the North Pacific biota.

The North Pacific is the largest cold-water source of lineages spreading to other modern marine temperate biotas. How this status was achieved remains unclear. One hypothesis is that functional innovations of large effect, defined as departures from the norm in temperate clades and which confer competitive or defensive benefits, increase resource availability, and raise performance standards in the biota as a whole, evolved earlier and more frequently in the North Pacific than elsewhere in the temperate zone. In support of this hypothesis, phylogenetic and fossil evidence reveals 47 temperate marine innovations beginning in the latest Eocene, of which half arose in the North Pacific. Of the 22 innovations of large effect, 13 (39%) evolved in the North Pacific, including basal growth in kelps and bottom-feeding herbivory and durophagy in mammals. Temperate innovations in the Southern Hemisphere and the North Atlantic appeared later and were less consequential. Most other innovations arose in refuges where the risks of predation and competition are low. Among temperate marine biotas, the North Pacific has the highest incidence of unique innovations and the earliest origins of major breakthroughs, five of which spread elsewhere.

The sea as deathtrap: comment on a paper by miller and wiens.

Miller & Wiens (2017) claim that low marine as compared with terrestrial diversity results from more frequent extinctions and insufficient time for diversification in marine clades. Their data on marine amniotes are unrepresentative of marine diversity, their analysis of clade dynamics is flawed, and they ignore previously proposed explanations for the diversity difference.

Rarity and persistence.

Rarity is a population characteristic that is usually associated with a high risk of extinction. We argue here, however, that chronically rare species (those with low population densities over many generations across their entire ranges) may have individual-level traits that make populations more resistant to extinction. The major obstacle to persistence at low density is successful fertilisation (union between egg and sperm), and chronically rare species are more likely to survive when (1) fertilisation occurs inside or close to an adult, (2) mate choice involves long-distance signals, (3) adults or their surrogate gamete dispersers are highly mobile, or (4) the two sexes are combined in a single individual. In contrast, external fertilisation and wind- or water-driven passive dispersal of gametes, or sluggish or sedentary adult life habits in the absence of gamete vectors, appear to be incompatible with sustained rarity. We suggest that the documented increase in frequency of these traits among marine genera over geological time could explain observed secular decreases in rates of background extinction. Unanswered questions remain about how common chronic rarity actually is, which traits are consistently associated with chronic rarity, and how chronically rare species are distributed among taxa, and among the world's ecosystems and regions.

How the Land Became the Locus of Major Evolutionary Innovations.

Life originated in the sea and evolved its early metabolic pathways in water [1, 2]. Nevertheless, activities of organisms on land have influenced and enriched marine ecosystems with oxygen and nutrients for billions of years [3-7]. In contrast to the history of species diversity in the sea and on land [8-10] and the flows of resources within and between these two realms [11], little is known about the times and places of origin of major metabolic and ecological innovations during the Phanerozoic. Many innovations among multicellular organisms originated in the sea during or before the Cambrian, including predation and most of its variations, biomineralization, colonial or clonal growth, bioerosion, deposit feeding, bioturbation by animals, communication at a distance by vision and olfaction, photosymbiosis, chemosymbiosis, suspension feeding, osmotrophy, internal fertilization, jet propulsion, undulatory locomotion, and appendages for movement. Activity is less constrained in air than in the denser, more viscous medium of water [9, 12-14]. I therefore predict that high-performance metabolic and ecological innovations should predominantly originate on land after the Ordovician once organisms had conquered the challenges of life away from water and later appeared in the sea, either in marine-colonizing clades or by arising separately in clades that never left the sea. In support of this hypothesis, I show that 11 of 13 major post-Ordovician innovations appeared first or only on land. This terrestrial locus of innovation cannot be explained by the Cretaceous to recent expansion of diversity on land. It reveals one of several irreversible shifts in the history of life.