Multilevel Selection Framework Research Articles

The emergence of group fitness.

Whether and how selection can act on collectives rather than single entities has been a tumultuous issue in evolutionary biology for decades. Despite examples of multilevel selection, a simple framework is needed that makes explicit the constraints that lead to the emergence of a "group fitness function." We use evolutionary game theory to show that two constraints are sufficient for the emergence of a well-defined group fitness, which could even apply to multispecies groups. First, different parts of the group contribute to one another's growth via resources produced proportionally to the density of each resource producer (not the density of the population receiving benefits). Second, invading groups do not share these resources with resident groups. Jointly, these two constraints lead to the "entanglement" of invading individuals' outcomes such that individual fitness can no longer be defined and group fitness predicts evolutionary dynamics through the emergence of a higher level evolutionary individual. Group fitness is an emergent property, irreducible to the fitness of the group's parts and exhibiting downward causality on the parts. By formalizing group fitness as a model for evolutionary transitions in individuality, these results open up a broad class of models under the multilevel-selection framework.

Gazing into the anthosphere: considering how microbes influence floral evolution.

The flower is the hallmark of angiosperms and its evolution is key to their diversification. As knowledge of ecological interactions between flowers and their microbial communities (the anthosphere) expands, it becomes increasingly important to consider the evolutionary impacts of these associations and their potential eco-evolutionary dynamics. In this Viewpoint we synthesize current knowledge of the anthosphere within a multilevel selection framework and illustrate the potential for the extended floral phenotype (the phenotype expressed from the genes of the plant and its associated flowermicrobes) to evolve. We argue that flower microbes are an important, but understudied, axis of variation that shape floral trait evolution and angiosperm reproductive ecology. We highlight knowledge gaps and discuss approaches that are critical for gaining a deeper understanding of the role microbes play in mediating plant reproduction, ecology, and evolution.

Evolution of multicellularity: cheating done right

For decades Darwinian processes were framed in the form of the Lewontin conditions: reproduction, variation and differential reproductive success were taken to be sufficient and necessary. Since Buss (The evolution of individuality, Princeton University Press, Princeton, 1987) and the work of Maynard Smith and Szathmary (The major transitions in evolution, Oxford University Press, Oxford, 1995) biologists were eager to explain the major transitions from individuals to groups forming new individuals subject to Darwinian mechanisms themselves. Explanations that seek to explain the emergence of a new level of selection, however, cannot employ properties that would already have to exist on that level for selection to take place. Recently, Hammerschmidt et al. (Nature 515:75–79, 2014) provided a ‘bottom-up’ experiment corroborating much of the theoretical work Paul Rainey has done since 2003 on how cheats can play an important role in the emergence of new Darwinian individuals on a multicellular level. The aims of this paper are twofold. First, I argue for a conceptual shift in perspective from seeing cheats as (1) a ‘problem’ that needs to be solved for multi-cellularity to evolve to (2) the very ‘key’ for the evolution of multicellularity. Secondly, I illustrate the consequences of this shift for both theoretical and experimental work, arguing for a more prominent role of ecology and the multi-level selection framework within the debate then they currently occupy.

Applying a cultural multilevel selection framework to the adoption of sustainable management practices in California viticulture

In light of the ongoing environmental impacts of agriculture, understanding farmer adoption of sustainable management practices (SMPs) is an important priority. Relatively little work in agricultural adoption has explicitly examined the multilevel dynamics of adoption decision-making. Yet because many SMPs involve cooperative dilemmas—they are individually costly but provide group benefits—understanding the dynamics of both individual and group level behavioral change is critical. In this paper, we argue that cultural evolutionary theory is well suited to examining the emergence and spread of cooperative SMPs, and we illustrate this claim by applying a cultural multilevel selection (CMLS) framework to the adoption of SMPs on the part of winegrape growers in California, USA. Using survey data from over 800 winegrape growers in 3 regions, we estimate the individual-level costs and group-level benefits of 44 different SMPs. We then relate this to variation in their adoption within and between winegrape growing regions to characterize the scope for cultural group selection of the various practices. We also identify a number of mechanisms that might plausibly explain the observed patterns of variation, including various forms of cultural group selection. We highlight the added value of this perspective with respect to the established approaches and outline the data requirements for researchers to conduct similar studies in other settings. Our results underscore the potential for a cultural evolutionary perspective to shed light on the multiscale mechanisms driving adoption of SMPs and, more generally, the promise of cultural evolutionary approaches to supplement existing analytical toolkits in sustainability science.

Evidence of cultural group selection in territorial lobstering in Maine

Relatively little is known about how resource conservation practices and institutions emerge. We examine the historical emergence of territoriality and conservation rules in Maine’s lobstering industry, using a cultural evolutionary perspective. Cultural evolution suggests that cultural adaptations such as practices and institutions arise as a result of evolutionary selection pressure. The cultural multilevel selection framework of Waring et al. (Ecol Soc, 2015) further proposes that group cultural adaptations tend to emerge at a level of social organization corresponding to the underlying dilemma. Drawing on detailed history and ethnography, we conduct a retrospective assessment to determine which levels of social organization experienced selection pressures that might explain the emergence of lobstering territoriality and conservation practices we observe in history. The evidence strongly suggests that informal territoriality evolved by selection on harbor gang behavior, while some conservation practices spread via selection at other levels from individuals to regional lobstering zones. We identify two apparent historical shifts in the dominant level of selection for these practices over the history of the industry and discuss the implications of this trajectory for the evolution of lobster management in the Gulf of Maine.

Cultural evolution and US agricultural institutions: a historical case study of Maine\u2019s blueberry industry

This paper presents a study of the emergence of environmental management institutions in Maine’s blueberry industry. We follow a cultural evolutionary approach to understand the factors that influenced the emergence of these institutions in environmental collective action problems. Specifically, we use a cultural multilevel selection framework to explore the prediction that collective action and institutions of environmental management emerge when cultural selection is the strongest among social groups positioned to solve a given collective action problem. To do this, we construct an evidence typology suited for a historical evolutionary analysis. We find that the scale of cultural adaptation responded to scale of the most pressing adaptive problem. The case study provides support for the group-level selection theory of institutional evolution, and displays patterns of institutional adaptation that respond to changing conditions over time. We argue that the dominant level of selection concept in multilevel selection theory helps to clarify how matches and mismatches between resource scale and institutional scale arise. We conclude that cultural evolutionary theory provides a general causal framework for organizing evidence, and complements the study of environmental history, which provides the temporal depth needed to examine evolutionary hypotheses.

Mobility can promote the evolution of cooperation via emergent self-assortment dynamics.

The evolution of costly cooperation, where cooperators pay a personal cost to benefit others, requires that cooperators interact more frequently with other cooperators. This condition, called positive assortment, is known to occur in spatially-structured viscous populations, where individuals typically have low mobility and limited dispersal. However many social organisms across taxa, from cells and bacteria, to birds, fish and ungulates, are mobile, and live in populations with considerable inter-group mixing. In the absence of information regarding others’ traits or conditional strategies, such mixing may inhibit assortment and limit the potential for cooperation to evolve. Here we employ spatially-explicit individual-based evolutionary simulations to incorporate costs and benefits of two coevolving costly traits: cooperative and local cohesive tendencies. We demonstrate that, despite possessing no information about others’ traits or payoffs, mobility (via self-propulsion or environmental forcing) facilitates assortment of cooperators via a dynamically evolving difference in the cohesive tendencies of cooperators and defectors. We show analytically that this assortment can also be viewed in a multilevel selection framework, where selection for cooperation among emergent groups can overcome selection against cooperators within the groups. As a result of these dynamics, we find an oscillatory pattern of cooperation and defection that maintains cooperation even in the absence of well known mechanisms such as kin interactions, reciprocity, local dispersal or conditional strategies that require information on others’ strategies or payoffs. Our results offer insights into differential adhesion based mechanisms for positive assortment and reveal the possibility of cooperative aggregations in dynamic fission-fusion populations.

DEEP SOCIALITY

DEEP SOCIALITY

Evaluating the role of reproductive constraints in ant social evolution

The reproductive division of labour is a key feature of eusociality in ants, where queen and worker castes show dramatic differences in the development of their reproductive organs. To understand the developmental and genetic basis underlying this division of labour, we performed a molecular analysis of ovary function and germ cell development in queens and workers. We show that the processes of ovarian development in queens have been highly conserved relative to the fruitfly Drosophila melanogaster. We also identify specific steps during oogenesis and embryogenesis in which ovarian and germ cell development have been evolutionarily modified in the workers. These modifications, which we call 'reproductive constraints', are often assumed to represent neutral degenerations that are a consequence of social evolutionary forces. Based on our developmental and functional analysis of these constraints, however, we propose and discuss the alternative hypothesis that reproductive constraints represent adaptive proximate mechanisms or traits for maintaining social harmony in ants. We apply a multi-level selection framework to help understand the role of these constraints in ant social evolution. A complete understanding of how cooperation, conflict and developmental systems evolve in social groups requires a 'socio-evo-devo' approach that integrates social evolutionary and developmental biology.

Population structure influences sexual conflict in wild populations of water striders

In sexual conflict, aggressive males frequently diminish the long-term reproductive success of females in efforts to gain a short-term advantage over rival males. This short-term advantage can selectively favour high-exploitation males. However, just as the over-exploitation of resources can lead to local extinction, the over-exploitation of females in the form of harassment by aggressive males can yield similar consequences resulting in reduced female fecundity, increased female mortality and overall decline in mating activity. This outcome may often be prevented by selection acting at multiple levels of biological organization. Directional selection favouring aggressive exploitation within groups can be balanced by directional selection amongst groups opposing exploitation. Such between-group selection has recently been demonstrated in laboratory studies of water striders, where the conditional dispersal of individuals increased variation amongst groups and influenced the balance of selection toward reduced male aggression. This multilevel selection (MLS) framework also provides predictive value when investigating natural populations differing in their relative strength of selection within versus among groups. For water striders, the consequences of local exploitation cause fitness differences between groups, favouring less aggressive males. Inconsistently flowing ephemeral streams consist of isolated pools that prevent aggressive male water striders from escaping the consequences of local exploitation. We, therefore, predicted that inconsistently flowing ephemeral streams would favour the evolution of less aggressive males than would perennial streams, which allow aggressive males to move more freely and to escape the group-level costs of their aggression. Comparing two neighbouring streams during the mating season, we found that males dispersed naturally between pools at much higher rates in the perennial stream than in the ephemeral stream. As predicted, we found that males from the perennial stream were significantly more aggressive than those from the ephemeral stream. We also found that dispersers were significantly more aggressive than non-dispersers within each stream. These field results illustrate the relevance of the MLS framework in our understanding of the evolution of sexual conflict.

Why multilevel selection matters

In spite of its checkered intellectual history, and in spite of the myriad proposals of alternative models that claim both to account for the range of human behavior and to dispense with the need for selection above the organism level, a multilevel selection framework allowing for biological as well as cultural group selection remains the only coherent means of accounting for the persistence and spread of behavioral inclinations which, at least upon first appearance at low frequency, would have been biologically altruistic. This argument is advanced on three tracks: through a review of experimental and observational evidence inconsistent with a narrow version of rational choice theory, through a critique of models or explanations purporting to account for prosocial behavior through other means, and via elaboration of the mechanisms, plausibility, and intellectual history of biological group selection.