Relatedness,Conflict, and the Evolution of Eusociality

The evolution of sterile worker castes in eusocial insects was a major problem in evolutionary theory until Hamilton developed a method called inclusive fitness. He used it to show that sterile castes could evolve via kin selection, in which a gene for altruistic sterility is favored when the altruism sufficiently benefits relatives carrying the gene. Inclusive fitness theory is well supported empirically and has been applied to many other areas, but a recent paper argued that the general method of inclusive fitness was wrong and advocated an alternative population genetic method. The claim of these authors was bolstered by a new model of the evolution of eusociality with novel conclusions that appeared to overturn some major results from inclusive fitness. Here we report an expanded examination of this kind of model for the evolution of eusociality and show that all three of its apparently novel conclusions are essentially false. Contrary to their claims, genetic relatedness is important and causal, workers are agents that can evolve to be in conflict with the queen, and eusociality is not so difficult to evolve. The misleading conclusions all resulted not from incorrect math but from overgeneralizing from narrow assumptions or parameter values. For example, all of their models implicitly assumed high relatedness, but modifying the model to allow lower relatedness shows that relatedness is essential and causal in the evolution of eusociality. Their modeling strategy, properly applied, actually confirms major insights of inclusive fitness studies of kin selection. This broad agreement of different models shows that social evolution theory, rather than being in turmoil, is supported by multiple theoretical approaches. It also suggests that extensive prior work using inclusive fitness, from microbial interactions to human evolution, should be considered robust unless shown otherwise.     

Light,iron, Sam Granick and the origin of life

Living matter is an organized system which requires a continual flux of energy for its survival. As a working assumption, the flux of energy required for the origin of a self-duplicating cell is taken as the power required for the maintenance of a modern cell: 10 mW per g of carbon or some 10⁵ times the output per gram of the sun. Solar photochemistry supplies the energy for the continuing evolution of life and, by continuity, for its origin. The iron oxide-sulfide photosynthetic unit proposed by S. Granick 35 years ago was meant to supply this energy. The evolution of complex organic photosensitizers is rationalized by the Granick hypothesis that biosynthetic pathways recapitulate their evolution. These concepts are discussed in the context of the evolution of photosynthetic systems and the known properties of these pigments.     

Science, religion, and society: the problem of evolution in america

American resistance to accepting evolution is uniquely high among First World countries. This is due largely to the extreme religiosity of the United States, which is much higher than that of comparably advanced nations, and to the resistance of many religious people to the facts and supposed implications of evolution. The prevalence of religious belief in the United States suggests that outreach by scientists alone will not have a huge effect in increasing the acceptance of evolution, nor will the strategy of trying to convince the faithful that evolution is compatible with their religion. Because creationism is a symptom of religion, another strategy to promote evolution involves loosening the grip of faith on America. This is easier said than done, for recent sociological surveys show that religion is highly correlated with the dysfunctionality of a society, and various measures of societal health show that the United States is one of the most socially dysfunctional First World countries. Widespread acceptance of evolution in America, then, may have to await profound social change.     

Haplodiploidy, sex, and the evolution of pesticide resistance

The assumption that males and females are equally tolerant to pesticides in haplodiploid arthropods led to the prediction that the evolution of resistance is faster in haplodiploid than in diploid arthropods. However, in this review, it was found that the ratio of male to female tolerance is substantially smaller in haplodiploid than in diploid arthropods, indicating that resistance alleles are not strongly up-regulated in haploid males. In addition, males were generally less tolerant than females in both haplodiploid and diploid arthropods. Factors such as sexual size dimorphism and sex-dependent selection may account for the lower tolerance in males than in females. Little among-population variation in the ratio of male to female tolerance was found in three species. Moreover, the tolerance ratio generally remained unchanged by selection for resistance to pesticides, although significant among-species variation was present within arthropod orders. This indicates that sexual dimorphism in pesticide tolerance evolves at a slower rate than resistance to pesticides. Simulations considering between-sex differences in pesticide tolerance showed that resistance evolution can be slower in haplodiploids than in diploids. Recessive resistance, low male tolerance to pesticides, fitness costs expressed in males, and the use of refuges contributed in substantially delaying the evolution of resistance in haplodiploid arthropods. These findings cast a new perspective on the evolution of pesticide resistance in haplodiploid herbivores and natural enemies.     

Furcation, field-splitting, and the evolutionary origins of novelty in arthropod photoreceptors

Arthropod photoreceptor evolution is a prime example of how evolution has used existing components in the origin of new structures. Here, we outline a comparative approach to understanding the mutational origins of novel structures, describing multiple examples from arthropod photoreceptor evolution. We suggest that developmental mechanisms have often split photoreceptors during evolution (field-splitting) and we introduce “co-duplication” as a null model for the mutational origins of photoreceptor components. Under co-duplication, gene duplication events coincide with the origin of a higher level structure like an eye. If co-duplication is rejected for a component, that component probably came to be used in a new photoreceptor through regulatory mutations. If not rejected, a gene duplication mutation may have allowed the component to be used in a new structure. In multiple case studies in arthropod photoreceptor evolution, we consistently reject the null hypothesis of co-duplication of genetic components and photoreceptors. Nevertheless, gene duplication events have in some cases occurred later, allowing divergence of photoreceptors. These studies provide a new perspective on the evolution of arthropod photoreceptors and provide a comparative approach that generalizes to the study of any evolutionary novelty.     

Relatedness, phylogeny, and evolution of the fungi

Recent advances in fungal systematics are reviewed in relation to our previous studies. The usefulness of the integrated analysis of genotypic (especially 18S rRNA gene sequence comparisons) and phenotypic (especially ultrastructural and chemotaxonomic data) characters has been emphasized for the major groups and selected taxa of the fungi, and the impact to fungal systematics and evolution is discussed. Our noteworthy studies and findings are: 1) polyphyly of the chytridiomycetes and zygomycetes, 2) phylogenetic origin of the entomophthoralean fungi includingBasidiobolus, 3) detection of a major new lineage “Archiascomycetes,” comprisingTaphrina, Protomyces andSaitoella, Schizosaccharomyces, andPneumocystis, within the Ascomycota, and its phylogenetic and evolutionary significance, 4) polyphyletic origins of species in the anamorphic genusGeosmithia, and 5) phylogenetic placement ofMixia osmundae, species correctly and incorrectly assigned to the genusTaphrina, and basidiomyceotus yeasts. The newest 18S rDNA sequence-based neighbor-joining trees of the Ascomycota are demonstrated. “Traditional studies of evolution have amply demonstrated that evolution at the phenotypic level is characterized by adaptation and opportunism, irregularity in pace, and inequality of rates among lineages. In contrast, studies of molecular evolution have revealed quite different features characterized by changes that are conservative in nature, random in pattern (independent of phenotypic characters), and quite regular in pace with equal rates among diverge [sic] lineages for a given protein”. (Kimura, M. 1983. The neutral theory of molecular evolution, pp. 308–309, Cambridge University Press, Cambridge.) Recipient of the 2nd Mycological Society of Japan's Excellent Achievement Award, 1998; the awarding lecture was given at the 42nd Annual Meeting of the Mycological Society of Japan, 16 May, 1998, Kyoto University, Kyoto. This review is based mainly on the publications intended for the Award.     

Phylogeny and the modalities of acoustic diversification in extant Eneopterinae (Insecta, Orthoptera, Grylloidea, Eneopteridae)

Calling with a tegminal stridulatory apparatus is widespread in crickets. However, the evolution of cricket stridulums has been poorly studied and then only on the basis of prephylogenetic models, which are unable to account for the huge diversity recently documented for acoustic features in crickets. The present paper focuses on the evolution of acoustic devices in the subfamily Eneopterinae. This is the first attempt to reconstruct the phylogeny of a large and diverse cricket clade in order to analyze the evolution of emitting structures using precise homology statements. In the first step, we reconstruct the phylogeny of this clade using a morphological data set of 193 characters and 45 taxa. The resultant phylogeny supports the monophyly of the subfamily and that of the 13 genera represented by at least two species in our taxonomic sample. Phylogenetic relationships within the subfamily also support the definition of five tribes: Eurepini, Eneopterini, Nisitrini, Xenogryllini and Lebinthini. In the second step, the evolution of acoustic devices is studied by optimization of venation characters defined on precise homology statements. As hypothesized by previous authors, losses of acoustic communication occur independently in the course of eneopterine evolution; however, they happen abruptly with no intermediate state. Our results also document for the first time the modalities of forewing evolution: the diversification of male forewing venation originates from two processes, a continuous and regular modification process, responsible for slight venation change; and an irregular, more intense punctuated process, allowing the emergence of different venations. This diversification process with sudden changes could be related to the occurrence of acoustic novelties in advertisement calls.     

Allee effects, immigration, and the evolution of species' niches

Theoretical studies of adaptation to sink environments (with conditions outside the niche requirements of a species) have shown that immigration from source habitats can either facilitate or inhibit local adaptation. Here, we examine the influence of immigration on the evolution of local adaptation, given an Allee effect (i.e., at low densities, absolute fitness increases with population density). We consider a deterministic model for evolution at a haploid locus, and a stochastic individual-based model for evolution of a quantitative trait, and several kinds of Allee effects. We demonstrate that increased immigration can greatly facilitate adaptive evolution in the sink; with greater immigration, local population sizes rise, and because of the Allee effect, there is a positive indirect effect of immigration on local fitness. This makes it easier for alleles of modest effect to be captured by natural selection, transforming the sink into a locally adapted population that can persist without immigration.     

Darwin, historical biogeography, and the importance of overcoming binary opposites

It is well known that Darwin and Wallace came to discover the phenomenon of evolution through a historical approach to the geographical distribution of organisms. Before Darwin, evolution was a mere speculation that could be invoked to explain some facts. Darwin's biogeographical argument for evolution is based largely on three main explanatory hypotheses. The first is that the geographical distribution of organisms is historically informative. The second hypothesis is that long-distance dispersal over barriers is one main force (extinction is the other) that modifies the distribution of organisms. The third of Darwin's biogeographical hypotheses is that the factors that shape the distribution of organisms are mainly historical (large, often global and long temporal scales) rather than ecological (small spatial and short temporal scales). From the time of Darwin until now, a wide spectrum of biogeographical schools have provided new insights that challenge the central role of space, dispersal and history as the main explanatory hypotheses for the distribution of organisms, generating three binary opposites: (1) the spatial dimension of evolution: geographical distribution of organisms as historically informative vs. historically uninformative; (2) the processes that modify the geographical distribution of organisms: dispersal vs. vicariance; and (3) the explanation of geographical distribution: history vs. ecology. We analyse these three binary opposites to show that the components of each are complementary rather than antagonistic approaches to the study of biogeography.     

Host mortality, predation and the evolution of parasite virulence

One of the most accepted views in the theoretical literature on virulence evolution is that a parasite's virulence will evolve to higher levels when its host's background mortality rate increases. Surprisingly, however, although many sources of background mortality involve predation, there has not yet been any theoretical research that explicitly considers how the dynamics of this important ecological interaction affects virulence evolution. Here, we consider how predation affects virulence evolution by explicitly introducing a predator into a classical susceptible–infected–susceptible epidemiological model. We find that, contrary to previous predictions, different sources of host mortality affect virulence evolution in different ways. Moreover, the way in which virulence evolution is affected depends on how tightly coupled the predator's dynamics are to the host population, and this can result in somewhat counterintuitive results. For example, indirect ecological effects can cause elevated host mortality to result in the evolution of lower parasite virulence, even if this elevated mortality arises from factors unrelated to predation.     

Monogamy,strongly bonded groups,and the evolution of human social structure

Human social evolution has most often been treated in a piecemeal fashion, with studies focusing on the evolution of specific components of human society such as pair‐bonding, cooperative hunting, male provisioning, grandmothering, cooperative breeding, food sharing, male competition, male violence, sexual coercion, territoriality, and between‐group conflicts. Evolutionary models about any one of those components are usually concerned with two categories of questions, one relating to the origins of the component and the other to its impact on the evolution of human cognition and social life. Remarkably few studies have been concerned with the evolution of the entity that integrates all components, the human social system itself. That social system has as its core feature human social structure, which I define here as the common denominator of all human societies in terms of group composition, mating system, residence patterns, and kinship structures. The paucity of information on the evolution of human social structure poses substantial problems because that information is useful, if not essential, to assess both the origins and impact of any particular aspect of human society.     

The fundamental units,processes and patterns of evolution,and the Tree of Life conundrum

Background

The elucidation of the dominant role of horizontal gene transfer (HGT) in the evolution of prokaryotes led to a severe crisis of the Tree of Life (TOL) concept and intense debates on this subject.

Concept

Prompted by the crisis of the TOL, we attempt to define the primary units and the fundamental patterns and processes of evolution. We posit that replication of the genetic material is the singular fundamental biological process and that replication with an error rate below a certain threshold both enables and necessitates evolution by drift and selection. Starting from this proposition, we outline a general concept of evolution that consists of three major precepts.1. The primary agency of evolution consists of Fundamental Units of Evolution (FUEs), that is, units of genetic material that possess a substantial degree of evolutionary independence. The FUEs include both bona fide selfish elements such as viruses, viroids, transposons, and plasmids, which encode some of the information required for their own replication, and regular genes that possess quasi-independence owing to their distinct selective value that provides for their transfer between ensembles of FUEs (genomes) and preferential replication along with the rest of the recipient genome.2. The history of replication of a genetic element without recombination is isomorphously represented by a directed tree graph (an arborescence, in the graph theory language). Recombination within a FUE is common between very closely related sequences where homologous recombination is feasible but becomes negligible for longer evolutionary distances. In contrast, shuffling of FUEs occurs at all evolutionary distances. Thus, a tree is a natural representation of the evolution of an individual FUE on the macro scale, but not of an ensemble of FUEs such as a genome.3. The history of life is properly represented by the "forest" of evolutionary trees for individual FUEs (Forest of Life, or FOL). Search for trends and patterns in the FOL is a productive direction of study that leads to the delineation of ensembles of FUEs that evolve coherently for a certain time span owing to a shared history of vertical inheritance or horizontal gene transfer; these ensembles are commonly known as genomes, taxa, or clades, depending on the level of analysis. A small set of genes (the universal genetic core of life) might show a (mostly) coherent evolutionary trend that transcends the entire history of cellular life forms. However, it might not be useful to denote this trend "the tree of life", or organismal, or species tree because neither organisms nor species are fundamental units of life.

Conclusion

A logical analysis of the units and processes of biological evolution suggests that the natural fundamental unit of evolution is a FUE, that is, a genetic element with an independent evolutionary history. Evolution of a FUE on the macro scale is naturally represented by a tree. Only the full compendium of trees for individual FUEs (the FOL) is an adequate depiction of the evolution of life. Coherent evolution of FUEs over extended evolutionary intervals is a crucial aspect of the history of life but a "species" or "organismal" tree is not a fundamental concept.

Reviewers

This articles was reviewed by Valerian Dolja, W. Ford Doolittle, Nicholas Galtier, and William Martin

     

Scientific schools: traditions, dogmas, progress in the study of the brain evolution

The role of traditions, revision of dogmatic concepts, and emergence of novel theories in the investigations of the vertebrate brain evolution on the bases of modern neuroscientific data represent the objective of the present paper. Problems of homology, encephalization, recapitulation, dissolution, and the significance of their revision for understanding the brain evolution are considered. Arguments for equal importance in studying consequences of both phylogenetic and divergent adaptive evolution are presented. Comparative study of functional mechanisms is suggested as a perspective trend of the evolutionary physiology. It will be a valuable tool both for understanding the brain evolution and for applied investigations in neurobiology and medicine.     

Evolution, hypotheses, and the question of whether humans are still evolving

A central requirement of this journal is that ideas should be testable. Can evolutionary ideas be tested? Ones about the past evolutionary history can be, but only if the hypothesis extends beyond describing what has happened into its present day implications. Evolutionary mechanisms can clearly be tested if they apply to fast-growing species, or provide specific tests of outcomes that would not otherwise be expected. But the future path of evolution, and especially of human evolution, is a more fraught area. There are still strong selective pressures on humans even in the affluent, urban West, deriving from pre-reproductive mortality, family size and age, and reproductive success. I skim the evidence that all three factors have substantial genetic components, and hence are likely to be the subject of future human evolution, and challenge readers to consider what testable hypotheses about human evolution these forces suggest.     

Cooperation,clumping and the evolution of multicellularity

The evolution of multicellular organisms represents one of the major evolutionary transitions in the history of life. A potential advantage of forming multicellular clumps is that it provides an efficiency benefit to pre-existing cooperation, such as the production of extracellular ‘public goods’. However, this is complicated by the fact that cooperation could jointly evolve with clumping, and clumping could have multiple consequences for the evolution of cooperation. We model the evolution of clumping and a cooperative public good, showing that (i) when considered separately, both clumping and public goods production gradually increase with increasing genetic relatedness; (ii) in contrast, when the traits evolve jointly, a small increase in relatedness can lead to a major shift in evolutionary outcome—from a non-clumping state with low public goods production to a cooperative clumping state with high values of both traits; (iii) high relatedness makes it easier to get to the cooperative clumping state and (iv) clumping can be inhibited when it increases the number of cells that the benefits of cooperation must be shared with, but promoted when it increases relatedness between those cells. Overall, our results suggest that public goods sharing can facilitate the formation of well-integrated cooperative clumps as a first step in the evolution of multicellularity.     

Biotic interactions, rapid evolution, and the establishment of introduced species

The biotic environment can pose a challenge to introduced species; however, it is not known how rapid evolution in introduced and resident species influences the probability that the introduced species will become established. Here, we analyze the establishment phase of invasion with eco-evolutionary models of introduced species involved in predator-prey, mutualistic, or competitive interactions with a resident species. We find that, depending on the strength of the biotic interaction, establishment is impossible, guaranteed, or, in a narrow range, determined by genetic variation. Over this narrow range, rapid evolution of the introduced species always favors establishment, whereas resident evolution may either inhibit or facilitate establishment, depending on the interaction type. Coevolution can also either increase or decrease the chance of establishment, depending on the initial genotype frequencies as well as the interaction type. Our results suggest that the conditions under which genetic variation influences establishment success are limited, but they highlight the importance of considering the resident community's evolutionary response to introduced species as a component of its invasibility.     

A model of the evolution of dichogamy incorporating sex-ratio selection, anther-stigma interference, and inbreeding depression

Historically, explanations for the evolution of floral traits that reduce self-fertilization have tended to focus on selection to avoid inbreeding depression. However, there is growing support for the hypothesis that such traits also play a role in promoting efficient pollen dispersal by reducing anther-stigma interference. The relative importance of these two selective pressures is currently a popular topic of investigation. To date, there has been no theoretical exploration of the relative contributions of selection to avoid the genetic costs of self-fertilization and selection to promote efficient pollen dispersal on the evolution of floral traits. We developed a population genetic model to examine the influence of these factors on the evolution of dichogamy: the temporal separation of anther maturation and stigma receptivity. Our analysis indicates that anther-stigma interference can favor dichogamy even in the absence of in-breeding depression. Although anther-stigma interference and inbreeding depression are the key forces driving the initial evolution of dichogamy, selection to match the timing of pollen dispersal to the availability of ovules at the population level becomes a more potent force opposing the further evolution of dichogamy as the extent of temporal separation increases. This result may help to explain otherwise puzzling phenomena such as why dichogamy is rarely complete in nature and why dichogamy tends to be associated with asynchronous flower presentation.     

Movement patterns, social dynamics, and the evolution of cooperation

The structure of social interactions influences many aspects of social life, including the spread of information and behavior, and the evolution of social phenotypes. After dispersal, organisms move around throughout their lives, and the patterns of their movement influence their social encounters over the course of their lifespan. Though both space and mobility are known to influence social evolution, there is little analysis of the influence of specific movement patterns on evolutionary dynamics. We explored the effects of random movement strategies on the evolution of cooperation using an agent-based prisoner’s dilemma model with mobile agents. This is the first systematic analysis of a model in which cooperators and defectors can use different random movement strategies, which we chose to fall on a spectrum between highly exploratory and highly restricted in their search tendencies. Because limited dispersal and restrictions to local neighborhood size are known to influence the ability of cooperators to effectively assort, we also assessed the robustness of our findings with respect to dispersal and local capacity constraints. We show that differences in patterns of movement can dramatically influence the likelihood of cooperator success, and that the effects of different movement patterns are sensitive to environmental assumptions about offspring dispersal and local space constraints. Since local interactions implicitly generate dynamic social interaction networks, we also measured the average number of unique and total interactions over a lifetime and considered how these emergent network dynamics helped explain the results. This work extends what is known about mobility and the evolution of cooperation, and also has general implications for social models with randomly moving agents.