Physical constraints during Snowball Earth drive the evolution of multicellularity.

Molecular and fossil evidence suggests that complex eukaryotic multicellularity evolved during the late Neoproterozoic era, coincident with Snowball Earth glaciations, where ice sheets covered most of the globe. During this period, environmental conditions-such as seawater temperature and the availability of photosynthetically active light in the oceans-likely changed dramatically. Such changes would have had significant effects on both resource availability and optimal phenotypes. Here, we construct and apply mechanistic models to explore (i) how environmental changes during Snowball Earth and biophysical constraints generated selective pressures, and (ii) how these pressures may have had differential effects on organisms with different forms of biological organization. By testing a series of alternative-and commonly debated-hypotheses, we demonstrate how multicellularity was likely acquired differently in eukaryotes and prokaryotes owing to selective differences on their size due to the biophysical and metabolic regimes they inhabit: decreasing temperatures and resource availability instigated by the onset of glaciations generated selective pressures towards smaller sizes in organisms in the diffusive regime and towards larger sizes in motile heterotrophs. These results suggest that changing environmental conditions during Snowball Earth glaciations gave multicellular eukaryotes an evolutionary advantage, paving the way for the complex multicellular lineages that followed.

Adaptation to a Viscous Snowball Earth Ocean as a Path to Complex Multicellularity.

AbstractAnimals, fungi, and algae with complex multicellular bodies all evolved independently from unicellular ancestors. The early history of these major eukaryotic multicellular clades, if not their origins, co-occur with an extreme phase of global glaciations known as the Snowball Earth. Here, I propose that the long-term loss of low-viscosity environments due to several rounds global glaciation drove the multiple origins of complex multicellularity in eukaryotes and the subsequent radiation of complex multicellular groups into previously unoccupied niches. In this scenario, life adapts to Snowball Earth oceans by evolving large size and faster speeds through multicellularity, which acts to compensate for high-viscosity seawater and achieve fluid flow at sufficient levels to satisfy metabolic needs. Warm, low-viscosity seawater returned with the melting of the Snowball glaciers, and with it, by virtue of large and fast multicellular bodies, new ways of life were unveiled.

An ecological driver for the macroevolution of morphological polymorphism within colonial invertebrates.

Colonial marine invertebrates, such as corals and bryozoans, have modular growth. Individual modules within a colony are homologous to an individual solitary animal body. But in contrast to the predominately sexual origin of solitary animal bodies, modules within a colony are always produced asexually. The repetition of modules and the indeterminism of their organization gives colonies the ability to grow in ways solitary animals cannot. Colonial invertebrates consequently grow in such a way as to resemble weeds, bushes, or trees. The multitude of growth forms of colonial invertebrates arise from differences how individual colonies within a species tend to invest their energy into modular growth, persistence, asexual propagation, and sexual reproduction. Moreover, many colonial invertebrates possess several body types, morphological polymorphism among modules, where modules qualitatively differ in shape, size, and function. In this paper, I propose a mechanism that links the origin of novel body types to the evolution of life-history strategies among species. When colonies first evolve from solitary ancestors, the life-history strategy of the colony remains constrained by the life-history strategies of the individual modules within the colony until a new polymorph type evolves. The addition of novel body types within a colony introduces potential variation in life-history strategies. Colonies can then change strategies by regulating the frequencies of body types within the colony. This, along with the ability of body types to simplify their structure permits colonies to evolve more complex life-histories. Each new polymorph type that evolves permits more variation in colonial life-histories to exist.

Coloniality, clonality, and modularity in animals: The elephant in the room.

Nearly half of the animal phyla contain species that propagate asexually via agametic reproduction, often forming colonies of genetically identical modules, that is, ramets, zooids, or polyps. Clonal reproduction, colony formation, and modular organization have important consequences for many aspects of organismal biology. Theories in ecology, evolution, and development are often based on unitary and, mainly, strictly sexually reproducing organisms, and though colonial animals dominate many marine ecosystems and habitats, recognized concepts for the study of clonal species are often lacking. In this review, we present an overview of the study of colonial and clonal animals, from the historic interests in this subject to modern research in a range of topics, including immunology, stem cell biology, aging, biogeography, and ecology. We attempt to portray the fundamental questions lying behind the biology of colonial animals, focusing on how colonial animals challenge several dogmas in biology as well as the remaining puzzles still to be answered, of which there are many.

From the individual to the colony: Marine invertebrates as models to understand levels of biological organization.

The developmental and evolutionary principles of coloniality in marine animals remain largely unexplored. Although many common traits have evolved independently in different groups of colonial animals, questions about their significance for colonial life histories remain unanswered. In 2018 (Nov. 25 - Dec. 8), the inaugural course on the Evolution of Coloniality and Modularity took place at the Center for Marine Biology of the University of São Paulo (CEBIMAR-USP), Brazil. During the intensive two-week graduate-level course, we addressed some of the historical ideas about animal coloniality by focal studies in bryozoans, tunicates, cnidarians, and sponges. We discussed many historical hypotheses and ways to test these using both extant and paleontological data, and we carried direct observations of animal colonies in the different phyla to address questions about coloniality. We covered topics related to multi-level selection theory and studied colonial traits, including modular miniaturization, polymorphism, brooding, and allorecognition. Course participants carried out short research projects using local species of animals to address questions on allorecognition and regeneration in ascidians and sponges, fusion and chimerism in anthoathecate hydrozoans, and evolution of polymorphism in bryozoans. Although many questions remain unanswered, this course served as a foundation to continue to develop a developmental and evolutionary synthesis of clonal and modular development in colonial marine organisms.

Evolutionary Determinants of Morphological Polymorphism in Colonial Animals.

Colonial animals commonly exhibit morphologically polymorphic modular units that are phenotypically distinct and specialize in specific functional tasks. But how and why these polymorphic modules have evolved is poorly understood. Across colonial invertebrates, there is wide variation in the degree of polymorphism, from none in colonial ascidians to extreme polymorphism in siphonophores, such as the Portuguese man-of-war. Bryozoa are a phylum of exclusively colonial invertebrates that uniquely exhibit almost the entire range of polymorphism, from monomorphic species to others that rival siphonophores in their polymorphic complexity. Previous approaches to understanding the evolution of polymorphism have been based on analyses of (1) the functional role of polymorphs or (2) presumed evolutionary costs and benefits based on evolutionary theory that postulates polymorphism should be evolutionarily sustainable only in more stable environments because polymorphism commonly leads to the loss of feeding and sexual competence. Here we use bryozoans from opposite shores of the Isthmus of Panama to revisit the environmental hypothesis by comparison of faunas from distinct oceanographic provinces that differ greatly in environmental variability, and we then examine the correlations between the extent of polymorphism in relation to patterns of ecological succession and variation in life histories. We find no support for the environmental hypothesis. Distributions of the incidence of polymorphism in the oceanographically unstable Eastern Pacific are indistinguishable from those in the more stable Caribbean. In contrast, the temporal position of species in a successional sequence is collinear with the degree of polymorphism because species with fewer types of polymorphs are competitively replaced by species with higher numbers of polymorphs on the same substrata. Competitively dominant species also exhibit patterns of growth that increase their competitive ability. The association between degrees of polymorphism and variations in life histories is fundamental to understanding of the macroevolution of polymorphism.

Marine extinction risk shaped by trait-environment interactions over 500 million years.

Perhaps the most pressing issue in predicting biotic responses to present and future global change is understanding how environmental factors shape the relationship between ecological traits and extinction risk. The fossil record provides millions of years of insight into how extinction selectivity (i.e., differential extinction risk) is shaped by interactions between ecological traits and environmental conditions. Numerous paleontological studies have examined trait-based extinction selectivity; however, the extent to which these patterns are shaped by environmental conditions is poorly understood due to a lack of quantitative synthesis across studies. We conducted a meta-analysis of published studies on fossil marine bivalves and gastropods that span 458 million years to uncover how global environmental and geochemical changes covary with trait-based extinction selectivity. We focused on geographic range size and life habit (i.e., infaunal vs. epifaunal), two of the most important and commonly examined predictors of extinction selectivity. We used geochemical proxies related to global climate, as well as indicators of ocean acidification, to infer average global environmental conditions. Life-habit selectivity is weakly dependent on environmental conditions, with infaunal species relatively buffered from extinction during warmer climate states. In contrast, the odds of taxa with broad geographic ranges surviving an extinction (>2500 km for genera, >500 km for species) are on average three times greater than narrow-ranging taxa (estimate of odds ratio: 2.8, 95% confidence interval = 2.3-3.5), regardless of the prevailing global environmental conditions. The environmental independence of geographic range size extinction selectivity emphasizes the critical role of geographic range size in setting conservation priorities.

Equatorial decline of reef corals during the last Pleistocene interglacial.

The Last Interglacial (LIG; ca. 125,000 y ago) resulted from rapid global warming and reached global mean temperatures exceeding those of today. The LIG thus offers the opportunity to study how life may respond to future global warming. Using global occurrence databases and applying sampling-standardization, we compared reef coral diversity and distributions between the LIG and modern. Latitudinal diversity patterns are characterized by a tropical plateau today but were characterized by a pronounced equatorial trough during the LIG. This trough is governed by substantial range shifts away from the equator. Range shifts affected both leading and trailing edges of species range limits and were much more pronounced in the Northern Hemisphere than south of the equator. We argue that interglacial warming was responsible for the loss of equatorial diversity. Hemispheric differences in insolation during the LIG may explain the asymmetrical response. The equatorial retractions are surprisingly strong given that only small temperature changes have been reported in the LIG tropics. Our results suggest that the poleward range expansions of reef corals occurring with intensified global warming today may soon be followed by equatorial range retractions.

Differential niche dynamics among major marine invertebrate clades.

The degree to which organisms retain their environmental preferences is of utmost importance in predicting their fate in a world of rapid climate change. Notably, marine invertebrates frequently show strong affinities for either carbonate or terrigenous clastic environments. This affinity is due to characteristics of the sediments as well as correlated environmental factors. We assessed the conservatism of substrate affinities of marine invertebrates over geological timescales, and found that niche conservatism is prevalent in the oceans, and largely determined by the strength of initial habitat preference. There is substantial variation in niche conservatism among major clades with corals and sponges being among the most conservative. Time-series analysis suggests that niche conservatism is enhanced during times of elevated nutrient flux, whereas niche evolution tends to occur after mass extinctions. Niche evolution is not necessarily elevated in genera exhibiting higher turnover in species composition.

The evolutionary history of division of labour.

Functional specialization, or division of labour (DOL), of parts within organisms and colonies is common in most multi-cellular, colonial and social organisms, but it is far from ubiquitous. Several mechanisms have been proposed to explain the evolutionary origins of DOL; the basic feature common to all of them is that functional differences can arise easily. These mechanisms cannot explain the many groups of colonial and social animals that exhibit no DOL despite up to 500 million years of evolution. Here, I propose a new hypothesis, based on a multi-level selection theory, which predicts that a reproductive DOL is required to evolve prior to subsequent functional specialization. I test this hypothesis using a dataset consisting of the type of DOL for living and extinct colonial and social animals. The frequency distribution of DOL and the sequence of its acquisition confirm that reproductive specialization evolves prior to functional specialization. A corollary of this hypothesis is observed in colonial, social and also within multi-cellular organisms; those species without a reproductive DOL have a smaller range of internal variation, in terms of the number of polymorphs or cell types, than species with a reproductive DOL.

Long-term differences in extinction risk among the seven forms of rarity.

Rarity is widely used to predict the vulnerability of species to extinction. Species can be rare in markedly different ways, but the relative impacts of these different forms of rarity on extinction risk are poorly known and cannot be determined through observations of species that are not yet extinct. The fossil record provides a valuable archive with which we can directly determine which aspects of rarity lead to the greatest risk. Previous palaeontological analyses confirm that rarity is associated with extinction risk, but the relative contributions of different types of rarity to extinction risk remain unknown because their impacts have never been examined simultaneously. Here, we analyse a global database of fossil marine animals spanning the past 500 million years, examining differential extinction with respect to multiple rarity types within each geological stage. We observe systematic differences in extinction risk over time among marine genera classified according to their rarity. Geographic range played a primary role in determining extinction, and habitat breadth a secondary role, whereas local abundance had little effect. These results suggest that current reductions in geographic range size will lead to pronounced increases in long-term extinction risk even if local populations are relatively large at present.

Bryozoan revelations.

Bryozoans, simple invertebrates living on the sea floor, are emerging as a model system for understanding ecological and evolutionary processes on macroevolutionary scales.

Reproductive innovations and pulsed rise in plant complexity.

Morphological complexity is a notable feature of multicellular life, although whether it evolves gradually or in early bursts is unclear. Vascular plant reproductive structures, such as flowers, are familiar examples of complex morphology. In this study, we use a simple approach based on the number of part types to analyze changes in complexity over time. We find that reproductive complexity increased in two pulses separated by ~250 million years of stasis, including an initial rise in the Devonian with the radiation of vascular plants and a pronounced increase in the Late Cretaceous that reflects flowering plant diversification. These pulses are associated with innovations that increased functional diversity, suggesting that shifts in complexity are linked to changes in function regardless of whether they occur early or late in the history of vascular plants.

The role of extinction in large-scale diversity-stability relationships.

More-diverse communities are thought to be ecologically stable because a greater number of ecological interactions among members allows for the increases in robustness and resilience. Diversity-stability relationships have mostly been studied on short ecological time scales but one study has identified such patterns over million-year time scales in reef communities. Here we propose and test a hypothesis for the mechanism of large-scale diversity-stability relationships in reefs. The extinction of community members destabilizes the community as a whole, unless there is sufficient diversity to buffer the community from the stochastic loss of members, thereby preventing collapse. If genera have high extinction rates, any variation in diversity among communities will result in a diversity-stability relationship. Conversely, in the absence of other mechanisms, the stability of low extinction communities is expected to be independent of diversity. We compare the extinction rates of six reef-building metazoan taxa to patterns of reef community stability and reef volume. We find that extinction of reef-builders occurs independent of reef volume, and that the strength of the diversity-stability relationship varies positively with extinction rate.

How colonial animals evolve.

The evolution of modular colonial animals such as reef corals and bryozoans is enigmatic because of the ability for modules to proliferate asexually as whole colonies reproduce sexually. This reproductive duality creates an evolutionary tension between modules and colonies because selection operates at both levels. To understand how this evolutionary conflict is resolved, we compared the evolutionary potential of module- and colony-level traits in two species of the bryozoan Stylopoma, grown and bred in a common garden experiment. We find quantitatively distinct differences in the evolutionary potential of modular and colony traits. Contrary to solitary organisms, individual traits are not heritable from mother to daughter modules, but colony traits are strongly heritable from parent to offspring colonies. Colony-level evolution therefore dominates because no evolutionary change can accumulate among its modules.

Evolution: Serving Up Light.

Dinoflagellate algae form symbiotic partnerships with hosts from across a wide swath of the tree of life. New work shows that the genus Symbiodinium should now be considered a family, and importantly that the group is 110 million years older than previously thought. This expanded time period resolves long-standing questions about the evolution of photosymbiosis.

Extinctions. Paleontological baselines for evaluating extinction risk in the modern oceans.

Marine taxa are threatened by anthropogenic impacts, but knowledge of their extinction vulnerabilities is limited. The fossil record provides rich information on past extinctions that can help predict biotic responses. We show that over 23 million years, taxonomic membership and geographic range size consistently explain a large proportion of extinction risk variation in six major taxonomic groups. We assess intrinsic risk-extinction risk predicted by paleontologically calibrated models-for modern genera in these groups. Mapping the geographic distribution of these genera identifies coastal biogeographic provinces where fauna with high intrinsic risk are strongly affected by human activity or climate change. Such regions are disproportionately in the tropics, raising the possibility that these ecosystems may be particularly vulnerable to future extinctions. Intrinsic risk provides a prehuman baseline for considering current threats to marine biodiversity.

Implementation of RCGP guidelines for acute low back pain: a cluster randomised controlled trial.

BACKGROUND: The Royal College of General Practitioners (RCGP) has produced guidelines for the management of acute low back pain in primary care. AIM: To investigate the impact on patient management of an educational strategy to promote these guidelines among general practitioners (GPs). DESIGN OF STUDY: Group randomised controlled trial, using the health centre as the unit of randomisation. SETTING: Primary care teams in north-west England. METHOD: Twenty-four health centres were randomly allocated to an intervention or control arm. Practices in the intervention arm were offered outreach visits to promote national guidelines on acute low back pain, as well as access to fast-track physiotherapy and to a triage service for patients with persistent symptoms. RESULTS: Twenty-four centres were randomised. Two thousand, one hundred and eighty-seven eligible patients presented with acute low back pain during the study period: 1049 in the intervention group and 1138 in the control group. There were no significant differences between study groups in the proportion of patients who were referred for X-ray, issued with a sickness certificate, prescribed opioids or muscle relaxants, or who were referred to secondary care, but significantly more patients in the intervention group were referred to physiotherapy or the back pain unit (difference in proportion = 12.2%, 95% confidence interval [CI] = 2.8% to 21.6%). CONCLUSION: The management of patients presenting with low back pain to primary care was mostly unchanged by an outreach educational strategy to promote greater adherence to RCGP guidelines among GPs. An increase in referral to physiotherapy or educational programmes followed the provision of a triage service.

Species selection and the macroevolution of coral coloniality and photosymbiosis.

Differences in the relative diversification rates of species with variant traits are known as species selection. Species selection can produce a macroevolutionary change in the frequencies of traits by changing the relative number of species possessing each trait over time. But species selection is not the only process that can change the frequencies of traits, phyletic microevolution of traits within species and phylogenetic trait evolution among species, the tempo and mode of microevolution can also change trait frequencies. Species selection, phylogenetic, and phyletic processes can all contribute to large-scale trends, reinforcing or canceling each other out. Even more complex interactions among macroevolutionary processes are possible when multiple covarying traits are involved. Here I present a multilevel macroevolutionary framework that is useful for understanding how macroevolutionary processes interact. It is useful for empirical studies using fossils, molecular phylogenies, or both. I illustrate the framework with the macroevolution of coloniality and photosymbiosis in scleractinian corals using a time-calibrated molecular phylogeny. I find that standing phylogenetic variation in coloniality and photosymbiosis deflects the direction of macroevolution from the vector of species selection. Variation in these traits constrains species selection and results in a 200 million year macroevolutionary equilibrium.