Unpacking brown food‐webs: Animal trophic identity reflects rampant microbivory

Detritivory is the dominant trophic paradigm in most terrestrial, aquatic, and marine ecosystems, yet accurate measurement of consumer trophic position within detrital (=“brown”) food webs has remained unresolved. Measurement of detritivore trophic position is complicated by the fact that detritus is suffused with microbes, creating a detrital complex of living and nonliving biomass. Given that microbes and metazoans are trophic analogues of each other, animals feeding on detrital complexes are ingesting other detritivores (microbes), which should elevate metazoan trophic position and should be rampant within brown food webs. We tested these hypotheses using isotopic (¹⁵N) analyses of amino acids extracted from wild and laboratory‐cultured consumers. Vertebrate (fish) and invertebrate detritivores (beetles and moths) were reared on detritus, with and without microbial colonization. In the field, detritivorous animal specimens were collected and analyzed to compare trophic identities among laboratory‐reared and free‐roaming detritivores. When colonized by bacteria or fungi, the trophic positions of detrital complexes increased significantly over time. The magnitude of trophic inflation was mediated by the extent of microbial consumption of detrital substrates. When detrital complexes were fed to vertebrate and invertebrate animals, the consumers registered similar degrees of trophic inflation, albeit one trophic level higher than their diets. The wild‐collected detritivore fauna in our study exhibited significantly elevated trophic positions. Our findings suggest that the trophic positions of detrital complexes rise predictably as microbes convert nonliving organic matter into living microbial biomass. Animals consuming such detrital complexes exhibit similar trophic inflation, directly attributable to the assimilation of microbe‐derived amino acids. Our data demonstrate that detritivorous microbes elevate metazoan trophic position, suggesting that detritivory among animals is, functionally, omnivory. By quantifying the impacts of microbivory on the trophic positions of detritivorous animals and then tracking how these effects propagate “up” food chains, we reveal the degree to which microbes influence consumer groups within trophic hierarchies. The trophic inflation observed among our field‐collected fauna further suggests that microbial proteins represent an immense contribution to metazoan biomass. Collectively, these findings provide an empirical basis to interpret detritivore trophic identity, and further illuminate the magnitude of microbial contributions to food webs.     

Energetics of microbial food webs

The energetic demand of microorganisms in natural waters and the flux of energy between microorganisms and metazoans has been evaluated by empirical measurements in nature, in microcosms and mesocosms, and by simulation models. Microorganisms in temperate and tropical waters often use half or more of the energy fixed by photosynthesis. Most simulations and some experimental results suggest significant energy transfer to metazoans, but empirical evidence is mixed. Considerations of the range of growth yields of microorganisms and the number of trophic transfers among them indicate major energy losses within microbial food webs. Our ability to verify and quantify these processes is limited by the variability of assimilation efficiency and uncertainty about the structure of microbial food webs. However, even a two-step microbial chain is a major energy sink. As an energetic link to metazoans, the detritus food web is inefficient, and its significance may have been overstated. There is not enough bacterial biomass associated with detritus to support metazoan detritivores. Much detritus is digestible by metazoans directly. Thus, metazoans and bacteria may to a considerable degree compete for a common resource. Microorganisms, together with metazoans, are important to the stability of planktonic communities through their roles as rapid mineralizers of organic matter, releasing inorganic nutrients. The competition for organic matter and the resultant rapid mineralization help maintain stable populations of phytoplankton in the absence of advective nutrient supply. At temperatures near O °C, bacterial metabolism is suppressed more than is the rate of photosynthesis. As a result, the products of the spring phytoplankton bloom in high-temperate latitudes are not utilized rapidly by bacteria. At temperatures below 0°C microbial food webs are neither energy sinks or links: they are suppressed. Because the underlying mechanism of low-temperature inhibition is not known, we cannot yet generalize about this as a control of food web processes. Microorganisms may operate on several trophic levels simultaneously. Therefore, the realism of the trophic level concept and the reality of the use of ecological efficiency calculations in ecosystem models is questionable.     

Intraspecific variation in an Ediacaran skeletal metazoan: Namacalathus from the Nama Group,Namibia

Namacalathus hermanastes is one of the oldest known skeletal metazoans, found in carbonate settings of the terminal Ediacaran (~550–541 million years ago [Ma]). The palaeoecology of this widespread, goblet‐shaped, benthic organism is poorly constrained yet critical for understanding the dynamics of the earliest metazoan communities. Analysis of in situ assemblages from the Nama Group, Namibia (~548–541 Ma), shows that Namacalathus exhibited size variation in response to differing water depths, hydrodynamic conditions and substrate types. In low‐energy, inner ramp environments, Namacalathus attains the largest average sizes but grew in transient, loosely aggregating, monospecific aggregations attached to microbial mats. In high‐energy mid‐ramp reefs, Namacalathus spatially segregated into different palaeoecological habitats with distinct size distributions. In outer ramp environments, individuals were small and formed patchy, dense, monospecific aggregations attached to thin microbial mats. Asexual budding is common in all settings. We infer that variations in size distribution in Namacalathus reflect differences in habitat heterogeneity and stability, including the longevity of mechanically stable substrates and oxic conditions. In the Nama Group, long‐lived skeletal metazoan communities developed within topographically heterogeneous mid‐ramp reefs, which provided diverse mechanically stable microbial substrates in persistently oxic waters, while inner and outer ramp communities were often ephemeral, developing during fleeting episodes of either oxia and/or substrate stability. We conclude that Namacalathus, which forms a component of these communities in the Nama Group, was a generalist that adapted to various palaeoecological habitats within a heterogeneous ecosystem landscape where favourable conditions persisted, and was also able to opportunistically colonise transiently hospitable environments. These early skeletal metazoans colonised previously unoccupied substrates in thrombolitic reefs and other microbial carbonate settings, and while they experienced relatively low levels of interspecific competition, they were nonetheless adapted to the diverse environments and highly dynamic redox conditions present in the terminal Ediacaran.     

The Precambrian emergence of animal life: a geobiological perspective

The earliest record of animals (Metazoa) consists of trace and body fossils restricted to the last 35 Myr of the Precambrian. It has been proposed that animals arose much earlier and underwent significant evolution as a cryptic fauna; however, the need for any unrecorded prelude of significant duration has been disputed. In this context, we consider recent published research on the nature and chronology of the earliest fossil record of metazoans and on the molecular‐based analysis that yielded older dates for the appearance of major animal groups. We review recent work on the climatic, geochemical, and ecological events that preceded animal fossils and consider their portent for metazoan evolution. We also discuss inferences about the physiology and gene content of the last common ancestor of animals and their closest unicellular relatives. We propose that the recorded Precambrian evolution of animals includes three intervals of advancement that begin with sponge‐grade organisms, and that any preceding cryptic fauna would be no more complex than sponges. The molecular data do not require that more complex animals appeared well before the recognized fossil record; nor, however, do they rule the possibility out, particularly if the interval of simpler metazoan ancestors lasted no more than about 100 or 200 Myr. The geological record of abrupt changes in climate, biogeochemistry, and phytoplankton diversity can be taken to be the result of changes in the carbon cycle triggered by the appearance and diversification of metazoans in an organic carbon‐rich ocean, but as yet no compelling evidence exists for this interpretation. By the end of this cryptic period, animals would already have possessed sophisticated systems of cell–cell signalling, adhesion, apoptosis, and segregated germ cells, possibly with a rudimentary body plan based on anterior–posterior organization. The controls on the timing and tempo of the earliest steps in metazoan evolution are unknown, but it seems likely that oxygen was a key factor in later diversification and increase in body size. We consider several recent scenarios describing how oxygen increased near the end of the Precambrian and propose that grazing and filter‐feeding animals depleted a marine reservoir of suspended organic matter, releasing a microbial ‘clamp’ on atmospheric oxygen.     

Trophic coupling of the microbial and the classical food web in Lake Baikal,Siberia

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Choanoflagellates, choanocytes, and animal multicellularity

Abstract. It is widely accepted that multicellular animals (metazoans) constitute a monophyletic unit, deriving from ancestral choanoflagellate‐like protists that gave rise to simple choanocyte‐bearing metazoans. However, a re‐assessment of molecular and histological evidence on choanoflagellates, sponge choanocytes, and other metazoan cells reveals that the status of choanocytes as a fundamental cell type in metazoan evolution is unrealistic. Rather, choanocytes are specialized cells that develop from non‐collared ciliated cells during sponge embryogenesis. Although choanocytes of adult sponges have no obvious homologue among metazoans, larval cells transdifferentiating into choanocytes at metamorphosis do have such homologues. The evidence reviewed here also indicates that sponge larvae are architecturally closer than adult sponges to the remaining metazoans. This may mean that the basic multicellular organismal architecture from which diploblasts evolved, that is, the putative planktonic archimetazoan, was more similar to a modern poriferan larva lacking choanocytes than to an adult sponge. Alternatively, it may mean that other metazoans evolved from a neotenous larva of ancient sponges. Indeed, the Porifera possess some features of intriguing evolutionary significance: (1) widespread occurrence of internal fertilization and a notable diversity of gastrulation modes, (2) dispersal through architecturally complex lecithotrophic larvae, in which an ephemeral archenteron (in dispherula larvae) and multiciliated and syncytial cells (in trichimella larvae) occur, (3) acquisition of direct development by some groups, and (4) replacement of choanocyte‐based filter‐feeding by carnivory in some sponges. Together, these features strongly suggest that the Porifera may have a longer and more complicated evolutionary history than traditionally assumed, and also that the simple anatomy of modern adult sponges may have resulted from a secondary simplification. This makes the idea of a neotenous evolution less likely than that of a larva‐like choanocyte‐lacking archimetazoan. From this perspective, the view that choanoflagellates may be simplified sponge‐derived metazoans, rather than protists, emerges as a viable alternative hypothesis. This idea neither conflicts with the available evidence nor can be disproved by it, and must be specifically re‐examined by further approaches combining morphological and molecular information. Interestingly, several microbial lin°Cages lacking choanocyte‐like morphology, such as Corallochytrea, Cristidiscoidea, Ministeriida, and Mesomycetozoea, have recently been placed at the boundary between fungi and animals, becoming a promising source of information in addition to the choanoflagellates in the search for the unicellular origin of animal multicellularity.     

Paleobiological Perspectives on Early Eukaryotic Evolution

Eukaryotic organisms radiated in Proterozoic oceans with oxygenated surface waters, but, commonly, anoxia at depth. Exceptionally preserved fossils of red algae favor crown group emergence more than 1200 million years ago, but older (up to 1600–1800 million years) microfossils could record stem group eukaryotes. Major eukaryotic diversification ∼800 million years ago is documented by the increase in the taxonomic richness of complex, organic-walled microfossils, including simple coenocytic and multicellular forms, as well as widespread tests comparable to those of extant testate amoebae and simple foraminiferans and diverse scales comparable to organic and siliceous scales formed today by protists in several clades. Mid-Neoproterozoic establishment or expansion of eukaryophagy provides a possible mechanism for accelerating eukaryotic diversification long after the origin of the domain. Protists continued to diversify along with animals in the more pervasively oxygenated oceans of the Phanerozoic Eon.Eukaryotic organisms have a long evolutionary history, recorded, in part, by conventional and molecular fossils. For the Phanerozoic Eon (the past 542 million years), eukaryotic evolution is richly documented by the skeletons (and, occasionally, nonskeletal remains) of animals, as well as the leaves, stems, roots, and reproductive organs of land plants. Phylogenetic logic, however, tells us that eukaryotes must have a deeper history, one that began long before the first plant and animal fossils formed. To what extent does the geological record preserve aspects of deep eukaryotic history, and can the chemistry of ancient sedimentary rocks elucidate the environmental conditions under which the eukaryotic cell took shape?     

The origin of metazoan development: a palaeobiological perspective

The rapid diversification of early Metazoa remains one of the most puzzling events in the fossil record. Several models have been proposed to explain a critical aspect of this event: the origin of Metazoan development. These include the origin of the eukaryotic cell, environmental triggers, key innovations or selection among cell lineages. Here, the first three hypotheses are evaulated within a phylogenetic framework using fossil, molecular and developmental evidence. Many elements of metazoan development are widely distributed among unicellular eukaryotes, yet only 3 of the 23 multicellular eukaryotic lineages evolved complex development. Molecular evidence indicates the lineage leading to the eukaryotic cell is nearly as old as the eubacterial and archaebacterial lineages, although the symbiotic events established that the eukaryotic cell probably occurred about 1.5 billion years ago. Yet Metazoa did not appear until 1000 to 600 million years ago (Myr), suggesting the origin of metazoan development must be linked to either an environmental trigger, perhaps an increase in atmospheric oxygen, or key innovations such as the development of collagen. Yet the first model fails to explain the unique appearance of complex development in Metazoa, while the latter fails to explain the simultaneous diversification of several ‘protist’ groups along with the Metazoa. A more complete model of the origin of metazoan development combines environmental triggering of a series of innovations, with successive innovations generating radiations of metazoan clades as lineages breached functional thresholds. The elaboration of new cell classes and the appearance of such developmental innovations as cell sheets may have been of particular importance. Evolutionary biologists often implicitly assume that evolution is a uniformitarian, time-homogeneous process without strong temporal asymmetries in evolutionary mechanisms, rate or context. Yet evolutionary patterns do exhibit such asymmetries, raising the possibility that such innovations as metazoan development impose non-uniformities of evolutionary process.     

Molecular paleontology and complexity in the last eukaryotic common ancestor

Abstract

Eukaryogenesis, the origin of the eukaryotic cell, represents one of the fundamental evolutionary transitions in the history of life on earth. This event, which is estimated to have occurred over one billion years ago, remains rather poorly understood. While some well-validated examples of fossil microbial eukaryotes for this time frame have been described, these can provide only basic morphology and the molecular machinery present in these organisms has remained unknown. Complete and partial genomic information has begun to fill this gap, and is being used to trace proteins and cellular traits to their roots and to provide unprecedented levels of resolution of structures, metabolic pathways and capabilities of organisms at these earliest points within the eukaryotic lineage. This is essentially allowing a molecular paleontology. What has emerged from these studies is spectacular cellular complexity prior to expansion of the eukaryotic lineages. Multiple reconstructed cellular systems indicate a very sophisticated biology, which by implication arose following the initial eukaryogenesis event but prior to eukaryotic radiation and provides a challenge in terms of explaining how these early eukaryotes arose and in understanding how they lived. Here, we provide brief overviews of several cellular systems and the major emerging conclusions, together with predictions for subsequent directions in evolution leading to extant taxa. We also consider what these reconstructions suggest about the life styles and capabilities of these earliest eukaryotes and the period of evolution between the radiation of eukaryotes and the eukaryogenesis event itself.     

Microbial mat controls on infaunal abundance and diversity in modern marine microbialites

Microbialites are the most abundant macrofossils of the Precambrian. Decline in microbialite abundance and diversity during the terminal Proterozoic and early Phanerozoic has historically been attributed to the concurrent radiation of complex metazoans. Similarly, the apparent resurgence of microbialites in the wake of Paleozoic and Mesozoic mass extinctions is frequently linked to drastic declines in metazoan diversity and abundance. However, it has become increasing clear that microbialites are relatively common in certain modern shallow, normal marine carbonate environments—foremost the Bahamas. For the first time, we present data, collected from the Exuma Cays, the Bahamas, systematically characterizing the relationship between framework‐building cyanobacteria, microbialite fabrics, and microbialite‐associated metazoan abundance and diversity. We document the coexistence of diverse microbialite and infaunal metazoan communities and demonstrate that the predominant control upon both microbialite fabric and metazoan community structure is microbial mat type. These findings necessitate that we rethink prevalent interpretations of microbialite–metazoan interactions and imply that microbialites are not passive recipients of metazoan‐mediated alteration. Additionally, this work provides support for the theory that certain Precambrian microbialites may have been havens of early complex metazoan life, rather than bereft of metazoans, as has been traditionally envisaged.     

The Emergence of Predators in Early Life: There was No Garden of Eden

Background

Eukaryote cells are suggested to arise somewhere between 0.85∼2.7 billion years ago. However, in the present world of unicellular organisms, cells that derive their food and metabolic energy from larger cells engulfing smaller cells (phagocytosis) are almost exclusively eukaryotic. Combining these propositions, that eukaryotes were the first phagocytotic predators and that they arose only 0.85∼2.7 billion years ago, leads to an unexpected prediction of a long period (∼1–3 billion years) with no phagocytotes – a veritable Garden of Eden.

Methodology

We test whether such a long period is reasonable by simulating a population of very simple unicellular organisms - given only basic physical, biological and ecological principles. Under a wide range of initial conditions, cellular specialization occurs early in evolution; we find a range of cell types from small specialized primary producers to larger opportunistic or specialized predators.

Conclusions

Both strategies, specialized smaller cells and phagocytotic larger cells are apparently fundamental biological strategies that are expected to arise early in cellular evolution. Such early predators could have been ‘prokaryotes’, but if the earliest cells on the eukaryote lineage were predators then this explains most of their characteristic features.     

The development and diversification of Precambrian life

During the past decade, important strides have been made toward deciphering the paleobiology of the Precambrian Eon, the earliest seven-eighths of Earth history. This progress has accured chiefly from micropaleontological and organic geochemical studies of fine-grained, ancient cherts. Although understanding of the early biota—of its composition, diversity, paleocology and evolution—still remains far from adequate, three particularly significant generalizations have emerged: (i) Living systems were extant earlier than about 3000 m.y. ago; (ii) between about 3000 and 1000 m.y. ago, the Earth's biota was dominated by prokaryotic blue-green algae; and (iii) the development of the nucleated, eukaryotic cell type somewhat earlier than 1000 m.y. ago led to a stage of rapid diversification that culminated with the appearance of megascopic life near the close of the Precambrian. Consideration of these generalizations, and of the evidence bearing on them provides a ‘state-of-the-art’ assessment of the current status of Precambrian paleobiology.     

Phosphogenesis in the 2460 and 2728 million‐year‐old banded iron formations as evidence for biological cycling of phosphate in the early biosphere

The banded iron formation deposited during the first 2 billion years of Earth's history holds the key to understanding the interplay between the geosphere and the early biosphere at large geological timescales. The earliest ore‐scale phosphorite depositions formed almost at ~2.0–2.2 billion years ago bear evidence for the earliest bloom of aerobic life. The cycling of nutrient phosphorus and how it constrained primary productivity in the anaerobic world of Archean–Palaeoproterozoic eons are still open questions. The controversy centers about whether the precipitation of ultrafine ferric oxyhydroxide due to the microbial Fe(II) oxidation in oceans earlier than 1.9 billion years substantially sequestrated phosphate, and whether this process significantly limited the primary productivity of the early biosphere. In this study, we report apatite radial flowers of a few micrometers in the 2728 million‐year‐old Abitibi banded iron formation and the 2460 million‐year‐old Kuruman banded iron formation and their similarities to those in the 535 million‐year‐old Lower Cambrian phosphorite. The lithology of the 535 Million‐year‐old phosphorite as a biosignature bears abundant biomarkers that reveal the possible similar biogeochemical cycling of phosphorus in the Later Archean and Palaeoproterozoic oceans. These apatite radial flowers represent the primary precipitation of phosphate derived from the phytoplankton blooms in the euphotic zones of Neoarchean and Palaoeproterozoic oceans. The unbiased distributions of the apatite radial flowers within sub‐millimeter bands do not support the idea of an Archean Crisis of Phosphate. This is the first report of the microbial mediated mineralization of phosphorus before the Great Oxidation Event when the whole biosphere was still dominated by anaerobic microorganisms.     

Relating planktonic microbial food web structure in lentic freshwater ecosystems to water quality and land use

Relationships among picoplankton, protozoa, phytoplankton, plantnutrients, lake type, drainage basin morphology and land coverwere studied in 45 water bodies in South Island, New Zealandthat ranged from large, deep, ultra-oligotrophic lakes to shallow,macrophyte-dominated ponds and swamps. The biomasses of mostheterotrophic components of the pelagic microbial food webswere positively related to phytoplankton and features of thedrainage basin that enhanced nutrient input, and imply strongresource-driven structuring of pelagic microbial food webs.Prokaryotic picophytoplankton biomass was negatively relatedto indices of eutrophication, and the picoautotroph contributionto total microbial food web biomass declined with increasingtotal phosphorus concentration from 16.5% in deep lakes to <0.02%in swamps and ponds. Biomass ratios of (picoplankton plus protozoa):phytoplanktonranged from 40:60 in swamps and ponds to >70:30 in deep lakes,and indicate the potential importance of microbial food websin carbon transfer to higher trophic levels in deep, less productivelakes. Strong relationships exist between land use in the catchmentand pelagic microbial food web structure and biomass acrossa wide range in size and trophic state of water bodies in heterogeneouslandscapes.     

Proterozoic history and present state of cyanobacteria

The paper delves into the main regularities of the distribution of fossil microorganisms in Precambrian rocks, beginning from the Archean Eon about 3.5 billion years ago and ending in the Cambrian Period about 0.5 billion years ago. The paper analyzes facial peculiarities in the lateral differentiation of microfossils in Proterozoic basins and the main stages of temporal changes in fossil cyanobacterial communities, which are based on the irreversible succession of physicochemical conditions on the Earth and the evolution of eukaryotic microorganisms and their incorporation into prokaryotic ecosystems. To gain insight into Proterozoic fossil records, modern stratified cyanobacterial mats built up from layers of prokaryotes are considered. The analysis of phosphatization, carbonatization, and silification processes in modern algal-bacterial communities suggests that analogous processes took place in Proterozoic microbiotas. A comparison of modern and Precambrian living forms confirms the inference that cyanobacterial communities are very conservative and have changed insignificantly both morphologically and physiologically during the past two billion years.     

The Proterozoic History and Present State of Cyanobacteria

The paper delves into the main regularities of the distribution of fossil microorganisms in Precambrian rocks, beginning from the Archean Eon about 3.5 billion years ago and ending in the Cambrian Period about 0.5 billion years ago. The paper analyzes facial peculiarities in the lateral differentiation of microfossils in Proterozoic basins and the main stages of temporal changes in fossil cyanobacterial communities, which are based on the irreversible succession of physicochemical conditions on the Earth and the evolution of eukaryotic microorganisms and their incorporation into prokaryotic ecosystems. To gain insight into Proterozoic fossil record, modern stratified cyanobacterial mats built up from layers of prokaryotes are considered. The analysis of phosphatization, carbonatization, and silification processes in modern algal–bacterial communities suggests that analogous processes took place in Proterozoic microbiotas. A comparison of modern and Precambrian living forms confirms the inference that cyanobacterial communities are very conservative and have changed insignificantly both morphologically and physiologically during the past two billion years.     

Feeding response of a benthic copepod to ciliate prey type,prey concentration and habitat complexity

1. Protozoans are important consumers within microbial food webs and, in turn, they represent potential prey for small metazoans. However, feeding interactions within these food webs are rarely characterised and this is especially true for freshwater sediments. 2. We aimed to quantify the feeding links between a freshwater meiofaunal copepod and ciliates in two laboratory experiments. The first experiment addressed the response of Eucyclops serrulatus towards ciliate density and type (two ciliate species of the same genus differing in terms of body size). A second experiment assessed the effect of habitat structure on feeding rates by introducing different structural complexity into the feeding arena. In contrast to the first experiment, which was run only for one time period, this experiment also tested three different total feeding times (4, 7 and 9 h). 3. Eucyclops serrulatus exhibited high ingestion rates, with 3–69 ciliates copepod^?1 h^?1 consumed depending on food concentration, food type and habitat complexity. Copepods exhibited a preference for the smaller ciliate when total ciliate concentration was low, but selected both ciliates equally when food concentrations were medium or high. However, at very high food concentration, Eucyclops preferred the larger ciliate (which was 1/3 of its own body size), suggesting that the longer handling times of the larger prey are rewarding when the large prey is present in high numbers. In terms of total numbers consumed, copepods fed on more small ciliates, but in terms of carbon units both ciliates were selected equally when total prey concentration was low or medium. However, copepods derived more carbon from the larger prey at high and very high prey concentrations (up to 0.7 μgC out of a maximum of 1.1 μgC copepod^?1 h^?1). Habitat complexity influenced the feeding of copepods when it was observed over time. 4. The copepod–ciliate link is well known from the pelagic zone of both marine and freshwater habitats. We have shown its potential importance within the benthos, where it can be influenced by food identity, food quantity and possibly by habitat complexity.     

Does resource availability help determine the evolutionary route to multicellularity?

Genetic heterogeneity and homogeneity are associated with distinct sets of adaptive advantages and bottlenecks, both in developmental biology and population genetics. Whereas populations of individuals are usually genetically heterogeneous, most multicellular metazoans are genetically homogeneous. Observing that resource scarcity fuels genetic heterogeneity in populations, we propose that monoclonal development is compatible with the resource‐rich and stable internal environments that complex multicellular bodies offer. In turn, polyclonal development persists in tumors and in certain metazoans, both exhibiting a closer dependence on external resources. This eco‐evo‐devo approach also suggests that multicellularity may originally have emerged through polyclonal development in early metazoans, because of their reduced shielding from environmental fluctuations.     

Tyrosine kinase signaling and the emergence of multicellularity

Tyrosine phosphorylation is an essential element of signal transduction in multicellular animals. Although tyrosine kinases were originally regarded as specific to the metazoan lineage, it is now clear that they evolved prior to the split between unicellular and multicellular eukaryotes (≈600million years ago). Genome analyses of choanoflagellates and other protists show an abundance of tyrosine kinases that rivals the most complex animals. Some of these kinases are orthologs of metazoan enzymes (e.g., Src), but others display unique domain compositions not seen in any metazoan. Biochemical experiments have highlighted similarities and differences between the unicellular and multicellular tyrosine kinases. In particular, it appears that the complex systems of kinase autoregulation may have evolved later in the metazoan lineage.