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.

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.

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.

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.

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.

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.

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.

Approaching a state shift in Earth's biosphere.

Localized ecological systems are known to shift abruptly and irreversibly from one state to another when they are forced across critical thresholds. Here we review evidence that the global ecosystem as a whole can react in the same way and is approaching a planetary-scale critical transition as a result of human influence. The plausibility of a planetary-scale 'tipping point' highlights the need to improve biological forecasting by detecting early warning signs of critical transitions on global as well as local scales, and by detecting feedbacks that promote such transitions. It is also necessary to address root causes of how humans are forcing biological changes.

Plant defences on land and in water: why are they so different?

BACKGROUND: Plants (attached photosynthesizing organisms) are eaten by a wide variety of herbivorous animals. Despite a vast literature on plant defence, contrasting patterns of antiherbivore adaptation among marine, freshwater and land plants have been little noticed, documented or understood. SCOPE: Here I show how the surrounding medium (water or air) affects not only the plants themselves, but also the sensory and locomotor capacities of herbivores and their predators, and I discuss patterns of defence and host specialization of plants and herbivores on land and in water. I analysed the literature on herbivory with special reference to mechanical defences and sensory cues emitted by plants. Spines, hairs, asymmetrically oriented features on plant surfaces, and visual and olfactory signals that confuse or repel herbivores are common in land plants but rare or absent in water-dwelling plants. Small terrestrial herbivores are more often host-specific than their aquatic counterparts. I propose that patterns of selection on terrestrial herbivores and plants differ from those on aquatic species. Land plants must often attract animal dispersers and pollinators that, like their herbivorous counterparts, require sophisticated locomotor and sensory abilities. Plants counter their attractiveness to animal helpers by evolving effective contact defences and long-distance cues that mislead or warn herbivores. The locomotor and sensory world of small aquatic herbivores is more limited. These characteristics result from the lower viscosity and density of air compared with water as well as from limitations on plant physiology and signal transmission in water. Evolutionary innovations have not eliminated the contrasts in the conditions of life between water and land. CONCLUSION: Plant defence can be understood fully when herbivores and their victims are considered in the broader context of other interactions among coexisting species and of the medium in which these interactions occur.

The rise of ocean giants: maximum body size in Cenozoic marine mammals as an indicator for productivity in the Pacific and Atlantic Oceans.

Large consumers have ecological influence disproportionate to their abundance, although this influence in food webs depends directly on productivity. Evolutionary patterns at geologic timescales inform expectations about the relationship between consumers and productivity, but it is very difficult to track productivity through time with direct, quantitative measures. Based on previous work that used the maximum body size of Cenozoic marine invertebrate assemblages as a proxy for benthic productivity, we investigated how the maximum body size of Cenozoic marine mammals, in two feeding guilds, evolved over comparable temporal and geographical scales. First, maximal size in marine herbivores remains mostly stable and occupied by two different groups (desmostylians and sirenians) over separate timeframes in the North Pacific Ocean, while sirenians exclusively dominated this ecological mode in the North Atlantic. Second, mysticete whales, which are the largest Cenozoic consumers in the filter-feeding guild, remained in the same size range until a Mio-Pliocene onset of cetacean gigantism. Both vertebrate guilds achieved very large size only recently, suggesting that different trophic mechanisms promoting gigantism in the oceans have operated in the Cenozoic than in previous eras.

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.

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.

Global phylogeny and new classification of the Rapaninae (Gastropoda: Muricidae), dominant molluscan predators on tropical rocky seashores.

The monophyly of the muricid subfamily Rapaninae has recently been confirmed with molecular techniques, but its composition and the relationships among its constituent genera remain unclear. We use four genes (28S rRNA, 12S rRNA, 16S rRNA and cytochrome c oxidase subunit I, COI) to construct a Bayesian phylogeny of 80 rapanine species (73% of the approximately 109 currently accepted), representing 27 of the 31 nominal genera. This is the most complete phylogeny of this taxonomically confusing subfamily yet produced. We propose a revised phylogenetic classification of the Rapaninae, assigning the recognized species to 28 genera. Most of the morphologically-defined rapanine genera are considered valid, including Purpura, Drupa, Thais and Nassa, but many of them are here restricted or redefined so that they are monophyletic. In particular the familiar genus Thais is narrowly restricted to a single species. Many groups previously accepted as subgenera, including Mancinella, Vasula, Thalessa and Thaisella, are here accorded full generic rank. We describe one new genus, Indothais. While we do not formally alter species-level taxonomy, we show molecular evidence for two cryptic species and several instances of probable species synonymy. We estimate the age of diversification of the Rapaninae as Late Cretaceous (75.9 Ma) and of many of its genera as Miocene.

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.

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.

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.

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.