Evolution from mixed to fixed handedness in mirror-image flowers: insights from adaptive dynamics.

Mirror-image flowers (enantiostyly) involve a form of sexual asymmetry in which a flower's style is deflected either to the left or right side, with a pollinating anther orientated in the opposite direction. This curious floral polymorphism, which was known but not studied by Charles Darwin, occurs in at least 11 unrelated angiosperm families and represents a striking example of adaptive convergence in form and function associated with cross-pollination by insects. In several lineages, dimorphic enantiostyly (one stylar orientation per plant, both forms occurring within populations) has evolved from monomorphic enantiostyly, in which all plants can produce both style orientations. We use a modelling approach to investigate the emergence of dimorphic enantiostyly from monomorphic enantiostyly under gradual evolution. We show using adaptive dynamics that depending on the balance between inbreeding depression following geitonogamy, pollination efficiency and plant density, dimorphism can evolve from an ancestral monomorphic population. In general, the newly emergent dimorphic population is stable against invasion of a monomorphic mutant. However, our model predicts that under certain ecological conditions, e.g., a decline of pollinators, dimorphic enantiostyly may revert to a monomorphic state. We demonstrate using population genetics simulations that the observed evolutionary transitions are possible assuming a plausible genetic architecture.

Alterations of pleiotropic neuropeptide-receptor gene couples in Cetacea.

BACKGROUND: Habitat transitions have considerable consequences in organism homeostasis, as they require the adjustment of several concurrent physiological compartments to maintain stability and adapt to a changing environment. Within the range of molecules with a crucial role in the regulation of different physiological processes, neuropeptides are key agents. Here, we examined the coding status of several neuropeptides and their receptors with pleiotropic activity in Cetacea. RESULTS: Analysis of 202 mammalian genomes, including 41 species of Cetacea, exposed an intricate mutational landscape compatible with gene sequence modification and loss. Specifically for Cetacea, in the 12 genes analysed we have determined patterns of loss ranging from species-specific disruptive mutations (e.g. neuropeptide FF-amide peptide precursor; NPFF) to complete erosion of the gene across the cetacean stem lineage (e.g. somatostatin receptor 4; SSTR4). CONCLUSIONS: Impairment of some of these neuromodulators may have contributed to the unique energetic metabolism, circadian rhythmicity and diving response displayed by this group of iconic mammals.

Correlated evolution of conspicuous colouration and burrowing in crayfish.

Conspicuous colours have fascinated biologists for centuries, leading to research on the evolution and functional significance of colour traits. In many cases, research suggests that conspicuous colours are adaptive and serve a function in sexual or aposematic signalling. In other cases, a lack of evidence for the adaptive value of conspicuous colours garners interest from biologists, such as when organisms that live underground and are rarely exposed to the surface are nevertheless colourful. Here, we use phylogenetic comparative methods to investigate colour evolution throughout freshwater crayfishes that vary in burrowing ability. Within the taxa we analysed, conspicuous colours have evolved independently over 50 times, and these colours are more common in semi-terrestrial crayfishes that construct extensive burrows. The intuitive but not evolutionarily justified assumption when presented with these results is to assume that these colours are adaptive. But contrary to this intuition, we discuss the hypothesis that colouration in crayfish is neutral. Supporting these ideas, the small population sizes and reduced gene flow within semi-terrestrial burrowing crayfishes may lead to the fixation of colour-phenotype mutations. Overall, our work brings into question the traditional view of animal colouration as a perfectly adapted phenotype.

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.

The diversity of social complexity in termites.

Sociality underpins major evolutionary transitions and significantly influences the structure and function of complex ecosystems. Social insects, seen as the pinnacle of sociality, have traits like obligate sterility that are considered 'master traits', used as single phenotypic measures of this complexity. However, evidence is mounting that completely aligning both phenotypic and evolutionary social complexity, and having obligate sterility central to both, is erroneous. We hypothesize that obligate and functional sterility are insufficient in explaining the diversity of phenotypic social complexity in social insects. To test this, we explore the relative importance of these sterility traits in an understudied but diverse taxon: the termites. We compile the largest termite social complexity dataset to date, using specimen and literature data. We find that although functional and obligate sterility explain a significant proportion of variance, neither trait is an adequate singular proxy for the phenotypic social complexity of termites. Further, we show both traits have only a weak association with the other social complexity traits within termites. These findings have ramifications for our general comprehension of the frameworks of phenotypic and evolutionary social complexity, and their relationship with sterility.

Global analysis of Poales diversification - parallel evolution in space and time into open and closed habitats.

Poales are one of the most species-rich, ecologically and economically important orders of plants and often characterise open habitats, enabled by unique suites of traits. We test six hypotheses regarding the evolution and assembly of Poales in open and closed habitats throughout the world, and examine whether diversification patterns demonstrate parallel evolution. We sampled 42% of Poales species and obtained taxonomic and biogeographic data from the World Checklist of Vascular Plants database, which was combined with open/closed habitat data scored by taxonomic experts. A dated supertree of Poales was constructed. We integrated spatial phylogenetics with regionalisation analyses, historical biogeography and ancestral state estimations. Diversification in Poales and assembly of open and closed habitats result from dynamic evolutionary processes that vary across lineages, time and space, most prominently in tropical and southern latitudes. Our results reveal parallel and recurrent patterns of habitat and trait transitions in the species-rich families Poaceae and Cyperaceae. Smaller families display unique and often divergent evolutionary trajectories. The Poales have achieved global dominance via parallel evolution in open habitats, with notable, spatially and phylogenetically restricted divergences into strictly closed habitats.

Multiple transitions between realms shape relict lineages of Proteus cave salamanders.

In comparison to biodiversity on Earth's surface, subterranean biodiversity has largely remained concealed. The olm (Proteus anguinus) is one of the most enigmatic extant cave inhabitants, and until now little was known regarding its genetic structure and evolutionary history. Olms inhabit subterranean waters throughout the Dinaric Karst of the western Balkans, with a seemingly uniform phenotypic appearance of cave-specialized traits: an elongate body, snout and limbs, degenerated eyes and loss of pigmentation ("white olm"). Only a single small region in southeastern Slovenia harbours olms with a phenotype typical of surface animals: pigmented skin, eyes, a blunt snout and short limbs ("black olm"). We used a combination of mitochondrial DNA and genome-wide single nucleotide polymorphism data to investigate the molecular diversity, evolutionary history and biogeography of olms along the Dinaric Karst. We found nine deeply divergent species-level lineages that separated between 17 and 4 million years ago, while molecular diversity within lineages was low. We detected no signal of recent admixture between lineages and only limited historical gene flow. Biogeographically, the contemporaneous distribution of lineages mostly mirrors hydrologically separated subterranean environments, while the historical separation of olm lineages follows microtectonic and climatic changes in the area. The reconstructed phylogeny suggests at least four independent transitions to the cave phenotype. Two of the species-level lineages have miniscule ranges and may represent Europe's rarest amphibians. Their rarity and the decline in other lineages call for protection of their subterranean habitats.

Multispecies interactions shape the transition to multicellularity.

The origin of multicellularity transformed the adaptive landscape on Earth, opening diverse avenues for further innovation. The transition to multicellular life is understood as the evolution of cooperative groups which form a new level of individuality. Despite the potential for community-level interactions, most studies have not addressed the competitive context of this transition, such as competition between species. Here, we explore how interspecific competition shapes the emergence of multicellularity in an experimental system with two yeast species, Saccharomyces cerevisiae and Kluyveromyces lactis, where multicellularity evolves in response to selection for faster settling ability. We find that the multispecies context slows the rate of the transition to multicellularity, and the transition to multicellularity significantly impacts community composition. Multicellular K. lactis emerges first and sweeps through populations in monocultures faster than in cocultures with S. cerevisiae. Following the transition, the between-species competitive dynamics shift, likely in part to intraspecific cooperation in K. lactis. Hence, we document an eco-evolutionary feedback across the transition to multicellularity, underscoring how ecological context is critical for understanding the causes and consequences of innovation. By including two species, we demonstrate that cooperation and competition across several biological scales shapes the origin and persistence of multicellularity.

Spontaneous Emergence of Multicellular Heritability.

The major transitions in evolution include events and processes that result in the emergence of new levels of biological individuality. For collectives to undergo Darwinian evolution, their traits must be heritable, but the emergence of higher-level heritability is poorly understood and has long been considered a stumbling block for nascent evolutionary transitions. Using analytical models, synthetic biology, and biologically-informed simulations, we explored the emergence of trait heritability during the evolution of multicellularity. Prior work on the evolution of multicellularity has asserted that substantial collective-level trait heritability either emerges only late in the transition or requires some evolutionary change subsequent to the formation of clonal multicellular groups. In a prior analytical model, we showed that collective-level heritability not only exists but is usually more heritable than the underlying cell-level trait upon which it is based, as soon as multicellular groups form. Here, we show that key assumptions and predictions of that model are borne out in a real engineered biological system, with important implications for the emergence of collective-level heritability.

A coarse-graining account of individuality: how the emergence of individuals represents a summary of lower-level evolutionary processes.

Explaining the emergence of individuality in the process of evolution remains a challenge; it faces the difficulty of characterizing adequately what 'emergence' amounts to. Here, I present a pragmatic account of individuality in which I take up this challenge. Following this account, individuals that emerge from an evolutionary transition in individuality are coarse-grained entities: entities that are summaries of lower-level evolutionary processes. Although this account may prima facie appear to ultimately rely on epistemic considerations, I show that it can be used to vindicate the emergence of individuals in a quasi-ontological sense. To this end, I discuss a recent account of evolutionary transitions in individuality proposed by Godfrey-Smith and Kerr (Brit J Philos Sci 64(1):205-222, 2013) where a transition occurs through several stages, each with an accompanying model. I focus on the final stage where higher-level entities are ascribed a separate fitness parameter, while they were not in the previous stages. In light of my account, I provide some justification for why such a change in parameters is necessary and cannot be dismissed as merely epistemic.

Compositional shifts associated with major evolutionary transitions in plants.

Heterogeneity in gene trees, morphological characters, and composition has been associated with several major plant clades. Here, we examine heterogeneity in composition across a large transcriptomic dataset of plants to better understand whether locations of shifts in composition are shared across gene regions and whether directions of shifts within clades are shared across gene regions. We estimate mixed models of composition for both nucleotide and amino acids across a recent large-scale transcriptomic dataset for plants. We find shifts in composition across both nucleotide and amino acid datasets, with more shifts detected in nucleotides. We find that Chlorophytes and lineages within experience the most shifts. However, many shifts occur at the origins of land, vascular, and seed plants. While genes in these clades do not typically share the same composition, they tend to shift in the same direction. We discuss potential causes of these patterns. Compositional heterogeneity has been highlighted as a potential problem for phylogenetic analysis, but the variation presented here highlights the need to further investigate these patterns for the signal of biological processes.

An environmentally induced multicellular life cycle of a unicellular cyanobacterium.

Understanding the evolutionary transition to multicellularity is a key problem in biology.1,2,3,4 Nevertheless, the ecological conditions driving such transitions are not well understood. The first known transition to multicellularity occurred 2.5 billion years ago in cyanobacteria,5,6,7 and today's cyanobacteria are characterized by enormous morphological diversity. They range from unicellular species; unicellular cyanobacteria with packet-like phenotypes, e.g., tetrads; and simple filamentous species to highly differentiated filamentous species.8,9,10 The cyanobacterium Cyanothece sp. ATCC 51142, an isolate from the intertidal zone of the U.S. Gulf Coast,11 was classified as a unicellular species.12 We report a facultative life cycle of Cyanothece sp. in which multicellular filaments alternate with unicellular stages. In a series of experiments, we identified salinity and population density as environmental factors triggering the phenotypic switch between the two morphologies. Then, we used numerical models to test hypotheses regarding the nature of the environmental cues and the mechanisms underlying filament dissolution. While the results predict that the observed response is likely caused by an excreted compound in the medium, we cannot fully exclude changes in nutrient availability (as in Tuomi et al.13 and Matz and Jürgens14). The best-fit modeling results show a nonlinear effect of the compound, which is characteristic of density-dependent sensing systems.15,16 Furthermore, filament fragmentation is predicted to occur by connection cleavage rather than cell death of each alternating cell, which is supported by fluorescent and scanning electron microscopy results. The switch between unicellular and multicellular morphology constitutes an environmentally dependent life cycle that is likely an important step en route to permanent multicellularity.

Evolution of the Okvik/Old Bering Sea culture of the Bering Strait as a major transition.

Great transitions are thought to embody major shifts in locus of selection, labour diversification and communication systems. Such expectations are relevant for biological and cultural systems as decades of research has demonstrated similar dynamics within the evolution of culture. The evolution of the Neo-Inuit cultural tradition in the Bering Strait provides an ideal context for examination of cultural transitions. The Okvik/Old Bering Sea (Okvik/OBS) culture of Bering Strait is the first representative of the Neo-Inuit tradition. Archaeological evidence drawn for settlement and subsistence data, technological traditions and mortuary contexts suggests that Okvik/OBS fits the definition of a major transition given change in the nature of group membership (from families to political groups with social ranking), task organization (emergent labour specialization) and communication (advent of complex art forms conveying social and ideological information). This permits us to develop a number of implications about the evolutionary process recognizing that transitions may occur on three scales: (1) ephemeral variants, as for example, simple technological entities; (2) integrated systems, spanning modular technology to socio-economic strategies; and (3) simultaneous change across all scales with emergent properties. This article is part of the theme issue 'Human socio-cultural evolution in light of evolutionary transitions'.

The transition from animal to human culture-simulating the social protocell hypothesis.

The origin of human cumulative culture is commonly envisioned as the appearance (some 2.0-2.5 million years ago) of a capacity to faithfully copy the know-how that underpins socially learned traditions. While certainly plausible, this story faces a steep 'startup problem'. For example, it presumes that ape-like early Homo possessed specialized cognitive capabilities for faithful know-how copying and that early toolmaking actually required such a capacity. The social protocell hypothesis provides a leaner story, where cumulative culture may have originated even earlier-as cumulative systems of non-cumulative traditions ('institutions' and 'cultural lifestyles'), via an emergent group-level channel of cultural inheritance. This channel emerges as a side-effect of a specific but in itself unremarkable suite of social group behaviours. It is independent of faithful know-how copying, and an ancestral version is argued to persist in Pan today. Hominin cultural lifestyles would thereby have gained in complexity and sophistication, eventually becoming independent units of selection (socionts) via a cultural evolutionary transition in individuality, abstractly similar to the origin of early cells. We here explore this hypothesis by simulating its basic premises. The model produces the expected behaviour and reveals several additional and non-trivial phenomena as fodder for future work. This article is part of the theme issue 'Human socio-cultural evolution in light of evolutionary transitions'.

Communication for collaborative computation: two major transitions in human evolution.

This paper presents and defends the following theoretical arguments: (1) The uniqueness of the human condition lies in the fact that only humans engage in collaborative computation, where different individuals work together on shared computational challenges. Collaborative computation is the foundation of our cumulative cultures. (2) Collaborative computation requires individuals to engage in instructive communication, where senders do not just send messages to receivers-but also send them instructions that the receivers are obliged to follow in the course of computing the messages. (3) The process of human evolution was driven throughout by the invention and development of tools of instructive communication. (4) In this process, two separate major transitions should be identified. The first was made possible by the toolkit of representational gestures (pointing, eye contact, manual demonstration, pantomime and more) that Merlin Donald called the toolkit of mimesis. Mimesis allows for collaborative computation as long as the information requiring computation is available for direct experiencing by the participants. The second was made possible by language, the tool that allowed its users, for the first time, to engage in collaborative computations of information they did not experience together-through the systematic instruction of the mental computations of imagination. This article is part of the theme issue 'Human socio-cultural evolution in light of evolutionary transitions'.

The economic superorganism in the complexity of evolution.

The transition to grain agriculture restructured human societies, creating a new whole, an economic superorganism. Homo sapiens became expansionary, structurally interdependent in material life, and a duality between them and Earth was created that had not previously existed. Yet H. sapiens are not the only species to make the transition to agriculture. Cross-species comparisons create an opening for a movement toward a focus on the universal and powerful agricultural system as a unique expression of the evolution of species cooperation. This shifts the focus around human social evolution away from culture and toward the formation and power of the economic system that took hold with the cultivation of annual grains. The basic structure and dynamic to economic life that began with grain agriculture has endured for 10 000 years and the duality between humans and Earth established therein is now reaching an apogee with the spectre of climate change and the mass extinction of other species on Earth. In this light, the questions emerge: Is the agricultural revolution an evolutionary transition adequately captured in existing frameworks of human social evolution? Is the human capacity for culture sufficient to override the power and dynamic of the economic superorganism? This article is part of the theme issue 'Human socio-cultural evolution in light of evolutionary transitions'.

Steps to individuality in biology and culture.

Did human culture arise through an evolutionary transition in individuality (ETI)? To address this question, we examine the steps of biological ETIs to see how they could apply to the evolution of human culture. For concreteness, we illustrate the ETI stages using a well-studied example, the evolution of multicellularity in the volvocine algae. We then consider how those stages could apply to a cultural transition involving integrated groups of cultural traditions and the hominins that create and transmit traditions. We focus primarily on the early Pleistocene and examine hominin carnivory and the cultural change from Oldowan to Acheulean technology. We use Pan behaviour as an outgroup comparison. We summarize the important similarities and differences we find between ETI stages in the biological and cultural realms. As we are not cultural anthropologists, we may overlook or be mistaken in the processes we associate with each step. We hope that by clearly describing these steps to individuality and illustrating them with cultural principles and processes, other researchers may build upon our initial exercise. Our analysis supports the hypothesis that human culture has undergone an ETI beginning with a Pan-like ancestor, continuing during the Pleistocene, and culminating in modern human culture. This article is part of the theme issue 'Human socio-cultural evolution in light of evolutionary transitions'.

Can models of evolutionary transition clarify the debates over the Neolithic Revolution?

The 'Neolithic Revolution,' sometimes referred to as the emergence of agriculture at its earliest in the southern Levant, is the most significant shift in human history, shaping the world we live in today. Yet, after 100 years of study, its major cause, tempo (gradual or revolutionary), and impact of human intentionality remain disputed. Here, we examine the research potential of an evolutionary transition in individuality (ETI) to clarify this dramatic shift. Applying an ETI research perspective reveals how different causes and conditions lead to the same result, enabling a holistic view rather than a reduction of 'Neolithic' to 'agriculture,' or to one major climatic condition, inheritance system or standard evolutionary model, thus allowing us to clarify and bypass some of these heated, unresolved disputes. Additionally, unlike current archaeological emphasis on 'where,' 'when,' 'why' and 'how' questions, the ETI perspective offers a productive path for resolving a fundamental preliminary anomaly: why and how could the Neolithic lifeway evolve at all, given the selfish interest of individuals in a hunter-gatherer group? We do not intend to solve the shift to Neolithic lifeways, only to offer a fresh lens for examining it, emphasizing the relevance of tracking within and between group differences. This article is part of the theme issue 'Human socio-cultural evolution in light of evolutionary transitions'.

Human socio-cultural evolution in light of evolutionary transitions: introduction to the theme issue.

Human societies are no doubt complex. They are characterized by division of labour, multiple hierarchies, intricate communication networks and transport systems. These phenomena and others have led scholars to propose that human society may be, or may become, a new hierarchical level that may dominate the individual humans within it, similar to the relations between an organism and its cells, or an ant colony and its members. Recent discussions of the possibility of this major evolutionary transition in individuality (ETI) raise interesting and controversial questions that are explored in the present issue from four different complementary perspectives. (i) The general theory of ETIs. (ii) The unique aspects of cultural evolution. (iii) The evolutionary history and pre-history of humans. (iv) Specific routes of a possible human ETI. Each perspective uses different tools provided by different disciplines: biology, anthropology, cultural evolution, systems theory, psychology, economy, linguistics and philosophy of science. Altogether, this issue provides a broad and rich application of the notion of ETI to human past, present and perhaps also future evolution. It presents important case studies, new theoretical results and novel questions for future research. This article is part of the theme issue 'Human socio-cultural evolution in light of evolutionary transitions'.

Socially transferred materials: why and how to study them.

When biological material is transferred from one individual's body to another, as in ejaculate, eggs, and milk, secondary donor-produced molecules are often transferred along with the main cargo, and influence the physiology and fitness of the receiver. Both social and solitary animals exhibit such social transfers at certain life stages. The secondary, bioactive, and transfer-supporting components in socially transferred materials have evolved convergently to the point where they are used in applications across taxa and type of transfer. The composition of these materials is typically highly dynamic and context dependent, and their components drive the physiological and behavioral evolution of many taxa. Our establishment of the concept of socially transferred materials unifies this multidisciplinary topic and will benefit both theory and applications.