What is inclusive fitness theory, and what is it for?

Inclusive fitness theory is a cornerstone of modern evolutionary biology, yet critics contend it is not general but subject to serious limitations, and is ripe for replacement, for example by multilevel selection theory. These critics also question empirical predictions made using inclusive fitness theory, such as on sex allocation, and the use of statistical concepts in understanding responses to selection. Here I summarise recent resolutions of these criticisms, then discuss what inclusive fitness theory actually is and why it is useful for evolutionary biology. In doing so I focus on recent developments in evaluating causal explanations for social evolution, and the role of inclusive fitness theory in explaining group adaptations, including the major transitions to obligate eusociality and eukaryotic multicellularity

Geometry shapes evolution of early multicellularity

Organisms have increased in complexity through a series of major evolutionary transitions, in which formerly autonomous entities become parts of a novel higher-level entity. One intriguing feature of the higher-level entity after some major transitions is a division of reproductive labor among its lower-level units. Although it can have clear benefits once established, it is unknown how such reproductive division of labor originates. We consider a recent evolution experiment on the yeast Saccharomyces cerevisiae as a unique platform to address the issue of reproductive differentiation during an evolutionary transition in individuality. In the experiment, independent yeast lineages evolved a multicellular "snowflake-like'' cluster form in response to gravity selection. Shortly after the evolution of clusters, the yeast evolved higher rates of cell death. While cell death enables clusters to split apart and form new groups, it also reduces their performance in the face of gravity selection. To understand the selective value of increased cell death, we create a mathematical model of the cellular arrangement within snowflake yeast clusters. The model reveals that the mechanism of cell death and the geometry of the snowflake interact in complex, evolutionarily important ways. We find that the organization of snowflake yeast imposes powerful limitations on the available space for new cell growth. By dying more frequently, cells in clusters avoid encountering space limitations, and, paradoxically, reach higher numbers. In addition, selection for particular group sizes can explain the increased rate of apoptosis both in terms of total cell number and total numbers of collectives. Thus, by considering the geometry of a primitive multicellular organism we can gain insight into the initial emergence of reproductive division of labor during an evolutionary transition in individuality.Comment: 7 figure

Social Evolution: New Horizons

Cooperation is a widespread natural phenomenon yet current evolutionary thinking is dominated by the paradigm of selfish competition. Recent advanced in many fronts of Biology and Non-linear Physics are helping to bring cooperation to its proper place. In this contribution, the most important controversies and open research avenues in the field of social evolution are reviewed. It is argued that a novel theory of social evolution must integrate the concepts of the science of Complex Systems with those of the Darwinian tradition. Current gene-centric approaches should be reviewed and com- plemented with evidence from multilevel phenomena (group selection), the constrains given by the non-linear nature of biological dynamical systems and the emergent nature of dissipative phenomena.Comment: 16 pages 5 figures, chapter in forthcoming open access book "Frontiers in Ecology, Evolution and Complexity" CopIt-arXives 2014, Mexic

Superorganismality and caste differentiation as points of no return:how the major evolutionary transitions were lost in translation

Four decades of sociobiology have left us with multiple superorganism concepts that are mutually inconsistent and uninformative on how superorganismality originates. These ambiguities can be traced to a broadened concept ofeusociality that denied colonies with physically differentiated castes the special statusthat inspired August Weismann, William Morton Wheeler, Ronald A. Fisher and Julian S. Huxley to consider them as organism-analogs. The heuristic definitions of superorganismality that began to emerge in the 1980s have precluded proper appreciation of which social insect lineages made irreversible evolutionary transitions to superorganismality, andwhich did not. This has impeded straightforward connections between inclusive fitness theory and the major evolutionary transitions towards higher organizational complexity. We evaluate the history by which these inconsistencies accumulated, develop a common causeapproach for understanding the origins of all eukaryotic transitions in hierarchical complexity, and argue that they are directly comparable in inclusive fitness terms and do not require potential internal conflicts to be resolved first. We conclude that recurring controversies over the status of inclusive fitness theory emanate from the arbitrarily defined sociobiological concepts of superorganismality and eusociality, not from the theory itself. The sociobiology-inspired definition of eusociality lumps a diverse spectrum of social systems into a single category, which causes fundamental differences in commitment to social life to be overlooked. We argue that behavioral categories need to be defined and delineated from the presence or absence of distinct traits whose evolutionary origin and maintenance can be explained, and suggest that it is meaningless to ask how eusociality and other categories lacking rigorous definition evolved. Early 20th century naturalists and geneticists realized that the key traits for social insects are reproductive altruism and the irreversible acquisition of an unmated worker caste. Hamilton’s rule is almost universally accepted as the best approximate algorithm for understanding the evolution and maintenance of condition-dependent reproductive altruism, and can also be used to explain evolutionary transitions to unconditional differentiation of permanently unmated castes. The origin and elaboration of somatic tissues in multicellular eukaryotes can be understood in a fully analogous way

On the origin of biological construction, with a focus on multicellularity

Biology is marked by a hierarchical organization: all life consists of cells; in some cases, these cells assemble into groups, such as endosymbionts or multicellular organisms; in turn, multicellular organisms sometimes assemble into yet other groups, such as primate societies or ant colonies. The construction of new organizational layers results from hierarchical evolutionary transitions, in which biological units (e.g., cells) form groups that evolve into new units of biological organization (e.g., multicellular organisms). Despite considerable advances, there is no bottom-up, dynamical account of how, starting from the solitary ancestor, the first groups originate and subsequently evolve the organizing principles that qualify them as new units. Guided by six central questions, we propose an integrative bottom-up approach for studying the dynamics underlying hierarchical evolutionary transitions, which builds on and synthesizes existing knowledge. This approach highlights the crucial role of the ecology and development of the solitary ancestor in the emergence and subsequent evolution of groups, and it stresses the paramount importance of the life cycle: only by evaluating groups in the context of their life cycle can we unravel the evolutionary trajectory of hierarchical transitions. These insights also provide a starting point for understanding the types of subsequent organizational complexity. The central research questions outlined here naturally link existing research programs on biological construction (e.g., on cooperation, multilevel selection, self-organization, and development) and thereby help integrate knowledge stemming from diverse fields of biology

The coevolution of cooperation and dispersal in social groups and its implications for the emergence of multicellularity

<p>Abstract</p> <p>Background</p> <p>Recent work on the complexity of life highlights the roles played by evolutionary forces at different levels of individuality. One of the central puzzles in explaining transitions in individuality for entities ranging from complex cells, to multicellular organisms and societies, is how different autonomous units relinquish control over their functions to others in the group. In addition to the necessity of reducing conflict over effecting specialized tasks, differentiating groups must control the exploitation of the commons, or else be out-competed by more fit groups.</p> <p>Results</p> <p>We propose that two forms of conflict – access to resources within groups and representation in germ line – may be resolved in tandem through individual and group-level selective effects. Specifically, we employ an optimization model to show the conditions under which different within-group social behaviors (cooperators producing a public good or cheaters exploiting the public good) may be selected to disperse, thereby not affecting the commons and functioning as germ line. We find that partial or complete dispersal specialization of cheaters is a general outcome. The propensity for cheaters to disperse is highest with intermediate benefit:cost ratios of cooperative acts and with high relatedness. An examination of a range of real biological systems tends to support our theory, although additional study is required to provide robust tests.</p> <p>Conclusion</p> <p>We suggest that trait linkage between dispersal and cheating should be operative regardless of whether groups ever achieve higher levels of individuality, because individual selection will always tend to increase exploitation, and stronger group structure will tend to increase overall cooperation through kin selected benefits. Cheater specialization as dispersers offers simultaneous solutions to the evolution of cooperation in social groups and the origin of specialization of germ and soma in multicellular organisms.</p

Inclusive fitness and the major transitions in evolution

Inclusive fitness theory is the leading framework for explaining the major transitions in evolution, whereby free-living subunits (e.g. cells, organisms) have cooperated to form new, higher-level units (e.g. organisms, eusocial societies). The theory has attracted considerable controversy. From a brief survey of the controversy's present status, I conclude that inclusive fitness theory continues to provide both a concept and a principled modelling tool of value for understanding social evolution, including major transitions. Turning to new developments in the study of major transitions, I describe work defining the point of occurrence of major transitions and, from inclusive fitness theory, the required conditions. I also suggest that it remains important to understand the evolution of individuality that occurs beyond such thresholds