Does high relatedness promote cheater‐free multicellularity in synthetic lifecycles?

The evolution of multicellularity is one of the key transitions in evolution and requires extreme levels of cooperation between cells. However, even when cells are genetically identical, noncooperative cheating mutants can arise that cause a breakdown in cooperation. How then, do multicellular organisms maintain cooperation between cells? A number of mechanisms that increase relatedness amongst cooperative cells have been implicated in the maintenance of cooperative multicellularity including single‐cell bottlenecks and kin recognition. In this study, we explore how relatively simple biological processes such as growth and dispersal can act to increase relatedness and promote multicellular cooperation. Using experimental populations of pseudo‐organisms, we found that manipulating growth and dispersal of clones of a social amoeba to create high levels of relatedness was sufficient to prevent the spread of cheating mutants. By contrast, cheaters were able to spread under low‐relatedness conditions. Most surprisingly, we saw the largest increase in cheating mutants under an experimental treatment that should create intermediate levels of relatedness. This is because one of the factors raising relatedness, structured growth, also causes high vulnerability to growth rate cheaters.     

Pleiotropic constraints promote the evolution of cooperation in cellular groups

The evolution of cooperation in cellular groups is threatened by lineages of cheaters that proliferate at the expense of the group. These cell lineages occur within microbial communities, and multicellular organisms in the form of tumours and cancer. In contrast to an earlier study, here we show how the evolution of pleiotropic genetic architectures—which link the expression of cooperative and private traits—can protect against cheater lineages and allow cooperation to evolve. We develop an age-structured model of cellular groups and show that cooperation breaks down more slowly within groups that tie expression to a private trait than in groups that do not. We then show that this results in group selection for pleiotropy, which strongly promotes cooperation by limiting the emergence of cheater lineages. These results predict that pleiotropy will rapidly evolve, so long as groups persist long enough for cheater lineages to threaten cooperation. Our results hold when pleiotropic links can be undermined by mutations, when pleiotropy is itself costly, and in mixed-genotype groups such as those that occur in microbes. Finally, we consider features of multicellular organisms—a germ line and delayed reproductive maturity—and show that pleiotropy is again predicted to be important for maintaining cooperation. The study of cancer in multicellular organisms provides the best evidence for pleiotropic constraints, where abberant cell proliferation is linked to apoptosis, senescence, and terminal differentiation. Alongside development from a single cell, we propose that the evolution of pleiotropic constraints has been critical for cooperation in many cellular groups.

The evolution of cooperation in cellular groups is threatened by lineages of cheaters that proliferate at the expense of the group. In this study, an age-structured model of cellular groups shows that pleiotropy promotes the evolution of cooperation and may have been important for the origins of multicellularity.     

Mutation, multilevel selection, and the evolution of propagule size during the origin of multicellularity

Evolutionary transitions require the organization of genetic variation at two (or more) levels of selection so that fitness heritability may emerge at the new level. In this article, we consider the consequences for fitness variation and heritability of two of the main modes of reproduction used in multicellular organisms: vegetative reproduction and single-cell reproduction. We study a model where simple cell colonies reproduce by fragments or propagules of differing size, with mutations occurring during colony growth. Mutations are deleterious at the colony level but can be advantageous or deleterious at the cell level ("selfish" or "uniformly deleterious" mutants). Fragment size affects fitness in two ways: through a direct effect on adult group size (which in turn affects fitness) and by affecting the within- and between-group variances and opportunity for selection on mutations at the two levels. We show that the evolution of fragment size is determined primarily by its direct effects on group size except when mutations are selfish. When mutations are selfish, smaller propagule size may be selected, including single-cell reproduction, even though smaller propagule size has a direct fitness cost by virtue of producing smaller organisms, that is, smaller adult cell groups.     

The sociobiology of biofilms

Biofilms are densely packed communities of microbial cells that grow on surfaces and surround themselves with secreted polymers. Many bacterial species form biofilms, and their study has revealed them to be complex and diverse. The structural and physiological complexity of biofilms has led to the idea that they are coordinated and cooperative groups, analogous to multicellular organisms. We evaluate this idea by addressing the findings of microbiologists from the perspective of sociobiology, including theories of collective behavior (self-organization) and social evolution. This yields two main conclusions. First, the appearance of organization in biofilms can emerge without active coordination. That is, biofilm properties such as phenotypic differentiation, species stratification and channel formation do not necessarily require that cells communicate with one another using specialized signaling molecules. Second, while local cooperation among bacteria may often occur, the evolution of cooperation among all cells is unlikely for most biofilms. Strong conflict can arise among multiple species and strains in a biofilm, and spontaneous mutation can generate conflict even within biofilms initiated by genetically identical cells. Biofilms will typically result from a balance between competition and cooperation, and we argue that understanding this balance is central to building a complete and predictive model of biofilm formation.     

The Evolutionary Origin of Somatic Cells under the Dirty Work Hypothesis

Reproductive division of labor is a hallmark of multicellular organisms. However, the evolutionary pressures that give rise to delineated germ and somatic cells remain unclear. Here we propose a hypothesis that the mutagenic consequences associated with performing metabolic work favor such differentiation. We present evidence in support of this hypothesis gathered using a computational form of experimental evolution. Our digital organisms begin each experiment as undifferentiated multicellular individuals, and can evolve computational functions that improve their rate of reproduction. When such functions are associated with moderate mutagenic effects, we observe the evolution of reproductive division of labor within our multicellular organisms. Specifically, a fraction of the cells remove themselves from consideration as propagules for multicellular offspring, while simultaneously performing a disproportionately large amount of mutagenic work, and are thus classified as soma. As a consequence, other cells are able to take on the role of germ, remaining quiescent and thus protecting their genetic information. We analyze the lineages of multicellular organisms that successfully differentiate and discover that they display unforeseen evolutionary trajectories: cells first exhibit developmental patterns that concentrate metabolic work into a subset of germ cells (which we call “pseudo-somatic cells”) and later evolve to eliminate the reproductive potential of these cells and thus convert them to actual soma. We also demonstrate that the evolution of somatic cells enables phenotypic strategies that are otherwise not easily accessible to undifferentiated organisms, though expression of these new phenotypic traits typically includes negative side effects such as aging.     

Failure to fix nitrogen by non-reproductive symbiotic rhizobia triggers host sanctions that reduce fitness of their reproductive clonemates

The legume-rhizobia symbiosis is a classical mutualism where fixed carbon and nitrogen are exchanged between the species. Nonetheless, the plant carbon that fuels nitrogen (N(2)) fixation could be diverted to rhizobial reproduction by 'cheaters'--rhizobial strains that fix less N(2) but potentially gain the benefit of fixation by other rhizobia. Host sanctions can decrease the relative fitness of less-beneficial reproductive bacteroids and prevent cheaters from breaking down the mutualism. However, in certain legume species, only undifferentiated rhizobia reproduce, while only terminally differentiated rhizobial bacteroids fix nitrogen. Sanctions were, therefore, tested in two legume species that host non-reproductive bacteroids. We demonstrate that even legume species that host non-reproductive bacteroids, specifically pea and alfalfa, can severely sanction undifferentiated rhizobia when bacteroids within the same nodule fail to fix N(2). Hence, host sanctions by a diverse set of legumes play a role in maintaining N(2) fixation.     

HORIZONTAL GENE TRANSFER AND THE EVOLUTION OF BACTERIAL COOPERATION

Bacteria frequently exhibit cooperative behaviors but cooperative strains are vulnerable to invasion by cheater strains that reap the benefits of cooperation but do not perform the cooperative behavior themselves. Bacterial genomes often contain mobile genetic elements such as plasmids. When a gene for cooperative behavior exists on a plasmid, cheaters can be forced to cooperate by infection with this plasmid, rescuing cooperation in a population in which mutation or migration has allowed cheaters to arise. Here we introduce a second plasmid that does not code for cooperation and show that the social dilemma repeats itself at the plasmid level in both within‐patch and metapopulation scenarios, and under various scenarios of plasmid incompatibility. Our results suggest that although plasmid carriage of cooperative genes can provide a transient defense against defection in structured environments, plasmid and chromosomal defection remain the only stable strategies in an unstructured environment. We discuss our results in the light of recent bioinformatic evidence that cooperative genes are overrepresented on mobile elements.     

The costs and benefits of multicellular group formation in algae*

The first step in the evolution of complex multicellular organisms involves single cells forming a cooperative group. Consequently, to understand multicellularity, we need to understand the costs and benefits associated with multicellular group formation. We found that in the facultatively multicellular algae Chlorella sorokiniana: (1) the presence of the flagellate Ochromonas danica or the crustacean Daphnia magna leads to the formation of multicellular groups; (2) the formation of multicellular groups reduces predation by O. danica, but not by the larger predator D. magna; (3) under conditions of relatively low light intensity, where competition for light is greater, multicellular groups grow slower than single cells; (4) in the absence of live predators, the proportion of cells in multicellular groups decreases at a rate that does not vary with light intensity. These results can explain why, in cases such as this algae species, multicellular group formation is facultative, in response to the presence of predators.     

从合作的进化探讨植物与传粉者的相互作用

合作的进化为研究植物–传粉者相互关系提供了新的视角。植物与传粉者通过"报酬换服务"建立种间合作关系。这一合作关系从建立、维持到解体面临着3个关键问题:(1)在植物和传粉者不了解对方质量信息时,双方如何选择出最适伙伴,进而建立合作关系;(2)合作方如何限制欺骗策略(比如,盗蜜和欺骗性传粉)的扩散以维持合作关系;(3)什么过程可导致传粉合作关系的解体。植物与传粉者间信号博弈或筛选博弈可促进二者合作关系的建立。面对欺骗策略,传粉者和植物分别采用伙伴选择机制和防御机制加以应对。合作者与欺骗者的稳定共存也有助于植物–传粉者合作的维持。从合作转向对抗、转向新的伙伴和合作放弃3个过程可导致植物–传粉者的合作关系的解体。植物与传粉者合作关系的理论预期已经得到了部分实验结果支持,深化了我们对植物与传粉者合作过程中关键机制的理解。在今后的研究中,需要进一步探讨以下问题:(1)传粉者对植物信号诚实性的选择作用和植物对传粉者的筛选作用;(2)植物与传粉者各自应对欺骗策略的可能机制及其相对重要性;(3)合作者与欺骗者稳定共存的机制;(4)植物与传粉者合作系统对全球变化的响应。     

Cheater genotypes in the parthenogenetic ant Pristomyrmex punctatus

Cooperation is subject to cheating strategies that exploit the benefits of cooperation without paying the fair costs, and it has been a major goal of evolutionary biology to explain the origin and maintenance of cooperation against such cheaters. Here, we report that cheater genotypes indeed coexist in field colonies of a social insect, the parthenogenetic ant Pristomyrmex punctatus. The life history of this species is exceptional, in that there is no reproductive division of labour: all females fulfil both reproduction and cooperative tasks. Previous studies reported sporadic occurrence of larger individuals when compared with their nest-mates. These larger ants lay more eggs and hardly take part in cooperative tasks, resulting in lower fitness of the whole colony. Population genetic analysis showed that at least some of these large-bodied individuals form a genetically distinct lineage, isolated from cooperators by parthenogenesis. A phylogenetic study confirmed that this cheater lineage originated intraspecifically. Coexistence of cheaters and cooperators in this species provides a good model system to investigate the evolution of cooperation in nature.     

Multi-species outcomes in a common model of sympatric speciation

While models of sympatric speciation are motivated in part by multi-species adaptive radiations such as the Cameroon crater lake cichlids, existing models have focused on bifurcation into a single pair of daughter species. This paper shows that a familiar model of sympatric speciation, driven by intraspecific competition and assortative mating based on ecological characters values, can yield multiple daughter species if individual niche widths are sufficiently restricted. Surprisingly, the multi-species outcome is not produced by successive bifurcation events, but by simultaneous divergence resulting in a hard polytomy. This result is sensitive to a number of assumptions, whose violation may prevent speciation. In some cases when speciation fails, the population instead ends in a state that closely resembles incipient species pairs, with an ecological polymorphism and partial reproductive isolation. However, this polymorphism is stable and does not lead to complete reproductive isolation, suggesting that empirical cases of incipient species pairs may not always end in speciation.     

Multi-species biofilms defined from drinking water microorganisms provide increased protection against chlorine disinfection

A model biofilm, formed of multiple species from environmental drinking water, including opportunistic pathogens, was created to explore the tolerance of multi-species biofilms to chlorine levels typical of water-distribution systems. All species, when grown planktonically, were killed by concentrations of chlorine within the World Health Organization guidelines (0.2–5.0?mg?l^?1). Higher concentrations (1.6–40-fold) of chlorine were required to eradicate biofilm populations of these strains, ～70% of biofilms tested were not eradicated by 5.0?mg?l^?1 chlorine. Pathogenic bacteria within the model multi-species biofilms had an even more substantial increase in chlorine tolerance; on average ～700–1100?mg?l^?1 chlorine was required to eliminate pathogens from the biofilm, 50–300-fold higher than for biofilms comprising single species. Confocal laser scanning microscopy of biofilms showed distinct 3D structures and multiple cell morphologies and arrangements. Overall, this study showed a substantial increase in the chlorine tolerance of individual species with co-colonization in a multi-species biofilm that was far beyond that expected as a result of biofilm growth on its own.     

Topoisomerase I-DNA complexes contribute to arsenic trioxide-induced apoptosis

Topoisomerase I is an essential enzyme that relaxes DNA supercoiling by forming covalent DNA cleavage complexes, which are normally transient. Topoisomerase I-DNA complexes can be trapped by anticancer drugs (camptothecins) as well as by endogenous and exogenous DNA lesions. We show here that arsenic trioxide (a potent inducer of apoptosis that induces the intracellular accumulation of reactive oxygen species and targets mitochondria) induces cellular topoisomerase I cleavage complexes. Bcl-2 overexpression and quenching of reactive oxygen species, which prevent arsenic trioxide-induced apoptosis, also prevent the formation of topoisomerase I-DNA complexes, whereas enhancement of reactive oxygen species accumulation promotes these complexes. The caspase inhibitor, benzyloxycarbonyl-VAD partially prevents arsenic trioxide-induced topoisomerase I-DNA complexes and apoptosis, suggesting that activated caspases further maintain intracellular levels of reactive oxygen species that induce the formation of topoisomerase I-DNA complexes. Down-regulation of topoisomerase I expression decreases arsenic trioxide-induced apoptotic DNA fragmentation. Thus, we propose that arsenic trioxide induces topoisomerase I-DNA complexes that participate in chromatin fragmentation and programmed cell death during apoptosis.     

Defining species guilds in the Central Hardwood Forest,USA

Tree regeneration outcomes are challenging to generalize and difficult to predict. Many tree species can establish new propagules in a variety of post-disturbance environments and many different reproductive mechanisms may be used. In order to develop conceptual models that accurately reflect reproductive potential, we need a better understanding of the similarities in regeneration ecology among species. We used information from the forest ecology literature to evaluate the reproductive attributes of sixty-two tree species in the central hardwood region of the eastern United States. Each species was classified categorically for features such as flowering, seed production and dispersal, seed dormancy, germination requirements, seedling characteristics, and vegetative reproduction. Cluster analysis (Jaccard's similarity coefficient, complete linkage method) and ordination (homogeneity analysis) were used to separate nine groups (guilds) of species that had similar reproductive attributes. Individual attributes that had high variance in the first and second dimensions included: seed banking, seed dispersal, seedling shade tolerance, and seedbed requirements. Members of each guild had similar levels of reproductive specialization and guilds were either pioneer-like, opportunistic, or persistent. Pioneer guilds included: short-lived or fugitive species that colonize sites rapidly and are too shade intolerant to replace themselves; shade-tolerant species that colonize frequently disturbed sites; and stress-tolerant pioneers that survive on dry or nutrient-poor sites. Opportunistic guilds contained species that are remarkably versatile in their reproductive effort. The most flexible opportunists can colonize new sites, maintain seed in a seed bank, sprout from existing stems and persist as a seedling or sapling bank. Persistent guilds contain species that develop and maintain advance regeneration. These include: species with moderate understory tolerance that regenerate via cycles of dieback and resprouting; and more tolerant species that maintain seedling or sapling banks. Our regeneration guilds may provide a useful approach for more realistically representing large and diverse sets of tree species in forest ecosystem models.     

Concurrent coevolution of intra‐organismal cheaters and resisters

The evolution of multicellularity is a major transition that is not yet fully understood. Specifically, we do not know whether there are any mechanisms by which multicellularity can be maintained without a single‐cell bottleneck or other relatedness‐enhancing mechanisms. Under low relatedness, cheaters can evolve that benefit from the altruistic behaviour of others without themselves sacrificing. If these are obligate cheaters, incapable of cooperating, their spread can lead to the demise of multicellularity. One possibility, however, is that cooperators can evolve resistance to cheaters. We tested this idea in a facultatively multicellular social amoeba, Dictyostelium discoideum. This amoeba usually exists as a single cell but, when stressed, thousands of cells aggregate to form a multicellular organism in which some of the cells sacrifice for the good of others. We used lineages that had undergone experimental evolution at very low relatedness, during which time obligate cheaters evolved. Unlike earlier experiments, which found resistance to cheaters that were prevented from evolving, we competed cheaters and noncheaters that evolved together, and cheaters with their ancestors. We found that noncheaters can evolve resistance to cheating before cheating sweeps through the population and multicellularity is lost. Our results provide insight into cheater–resister coevolutionary dynamics, in turn providing experimental evidence for the maintenance of at least a simple form of multicellularity by means other than high relatedness.     

HOW TO PREVENT CHEATING: A DIGESTIVE SPECIALIZATION TIES MUTUALISTIC PLANT-ANTS TO THEIR ANT-PLANT PARTNERS

Mutualisms often involve reciprocal adaptations of both partners. Acacia ant-plants defended by symbiotic Pseudomyrmex ant mutualists secrete sucrose-free extrafloral nectar, which is unattractive to generalists. We aimed to investigate whether this extrafloral nectar can also exclude exploiters, that is nondefending ant species. Mutualist workers discriminated against sucrose whereas exploiters and generalists with no affinity toward Acacia myrmecophytes preferred sucrose, because mutualist workers lacked the sucrose-cleaving enzyme invertase, which is present in workers of the other two groups. Sucrose uptake induced invertase activity in workers of parasites and generalists, but not mutualists, and in larvae of all species: the mutualists loose invertase during their ontogeny. This reduced metabolic capacity ties the mutualists to their plant hosts, but it does not completely prevent the mutualism from exploitation. We therefore investigated whether the exploiters studied here are cheaters (i.e., have evolved from former mutualists) or parasites (exploiters with no mutualistic ancestor). A molecular phylogeny demonstrates that the exploiter species did not evolve from former mutualists, and no evidence for cheaters was found. We conclude that being specialized to their partner can prevent mutualists from becoming cheaters, whereas other mechanisms are required to stabilize a mutualism against the exploitation by parasites.     

LARGE POPULATION SIZE PREDICTS THE DISTRIBUTION OF ASEXUALITY IN SCALE INSECTS

Understanding why some organisms reproduce by sexual reproduction while others can reproduce asexually remains an important unsolved problem in evolutionary biology. Simple demography suggests that asexuals should outcompete sexually reproducing organisms, because of their higher intrinsic rate of increase. However, the majority of multicellular organisms have sexual reproduction. The widely accepted explanation for this apparent contradiction is that asexual lineages have a higher extinction rate. A number of models have indicated that population size might play a crucial role in the evolution of asexuality. The strength of processes that lead to extinction of asexual species is reduced when population sizes get very large, so that the long‐term advantage of sexual over asexual reproduction may become negligible. Here, we use a comparative approach using scale insects (Coccoidea, Hemiptera) to show that asexuality is indeed more common in species with larger population density and geographic distribution and we also show that asexual species tend to be more polyphagous. We discuss the implication of our findings for previously observed patterns of asexuality in agricultural pests.     

Thermodynamic perspectives on genetic instructions, the laws of biology and diseased states

This article examines in a broad perspective entropy and some examples of its relationship to evolution, genetic instructions and how we view diseases. Living organisms are programmed by functional genetic instructions (FGI), through cellular communication pathways, to grow and reproduce by maintaining a variety of hemistable, ordered structures (low entropy). Living organisms are far from equilibrium with their surrounding environmental systems, which tends towards increasing disorder (increasing entropy). Organisms free themselves from high entropy (high disorder) to maintain their cellular structures for a period of time sufficient to allow reproduction and the resultant offspring to reach reproductive ages. This time interval varies for different species. Bacteria, for example need no sexual parents; dividing cells are nearly identical to the previous generation of cells, and can begin a new cell cycle without delay under appropriate conditions. By contrast, human infants require years of care before they can reproduce. Living organisms maintain order in spite of their changing surrounding environment that decreases order according to the second law of thermodynamics. These events actually work together since living organisms create ordered biological structures by increasing local entropy. From a disease perspective, viruses and other disease agents interrupt the normal functioning of cells. The pressure for survival may result in mechanisms that allow organisms to resist attacks by viruses, other pathogens, destructive chemicals and physical agents such as radiation. However, when the attack is successful, the organism can be damaged until the cell, tissue, organ or entire organism is no longer functional and entropy increases.     

ON THE EVOLUTION OF DIFFERENTIATED MULTICELLULARITY

Most conspicuous organisms are multicellular and most multicellular organisms develop somatic cells to perform specific, nonreproductive tasks. The ubiquity of this division of labor suggests that it is highly advantageous. In this article I present a model to study the evolution of specialized cells. The model allows for unicellular and multicellular organisms that may contain somatic (terminally differentiated) cells. Cells contribute additively to a quantitative trait. The fitness of the organism depends on this quantitative trait (via a benefit function), the size of the organism, and the number of somatic cells. The model allows one to determine when somatic cells are advantageous and to calculate the optimum number (or fraction) of reproductive cells. I show that the fraction of reproductive cells is always surprisingly high. If somatic cells are very small, they can outnumber reproductive cells but their biomass is still less than the biomass of reproductive cells. I discuss the biology of primitive multicellular organisms with respect to the model predictions. I find a good agreement and outline how this work can be used to guide further quantitative studies of multicellularity.