Ashleigh S. Griffin

• University of Oxford

Phylogenetic comparative methods are important tools in biology, providing insights into the way traits evolve. There are many technical resources describing how these methods work. Our aim here is to complement these with an overview of the types of biological questions that can be addressed by different methods and to outline potential pitfalls a...

Hamilton’s rule provides the cornerstone for our understanding of the evolution of all forms of social behavior, from altruism to spite, across all organisms, from viruses to humans. In contrast to the standard prediction from Hamilton’s rule, recent studies have suggested that altruistic helping can be favored even if it does not benefit relatives...

The growth and success of many bacteria appear to rely on a stunning range of cooperative behaviours. But what is cooperation and how is it studied?

Antimicrobial resistance poses an escalating global threat, rendering traditional drug development approaches increasingly ineffective. Thus, novel alternatives to antibiotic-based therapies are needed. Exploiting pathogen cooperation as a strategy for combating resistant infections has been proposed but lacks experimental validation. Empirical fin...

Obligately multicellular organisms, where cells can only reproduce as part of the group, have evolved multiple times across the tree of life. Obligate multicellularity has only evolved when clonal groups form by cell division, rather than by cells aggregating, as clonality prevents internal conflict. Yet obligately multicellular organisms still var...

Pathogenic bacteria respond to antibiotic pressure with the evolution of resistance but survival can also depend on their ability to tolerate antibiotic treatment, known as tolerance. While a variety of resistance mechanisms and underlying genetics are well characterized in vitro and in vivo, an understanding of the evolution of tolerance, and how...

For infections to be maintained in a population, pathogens must compete to colonize hosts and transmit between them. We use an experimental approach to investigate within-and-between host dynamics using the pathogen Pseudomonas aeruginosa and the animal host Caenorhabditis elegans. Within-host interactions can involve the production of goods that a...

Metazoans function as individual organisms but also as “colonies” of cells whose single-celled ancestors lived and reproduced independently. Insights from evolutionary biology about multicellular group formation help us understand the behavior of cells: why they cooperate, and why cooperation sometimes breaks down. Current explanations for multicel...

Bacteriocins are antimicrobial toxins produced by bacteria to defend and invade territories by killing unrelated strains and species. Understanding if bacteriocins shape natural populations is important for understanding the evolution of antimicrobial resistance and identifying novel antimicrobials for clinical use. Staphylococcus aureus is an oppo...

Bacteria use type VI secretion systems (T6SSs) to deliver effector proteins into other cells or the extracellular space. Those effectors kill microbes, manipulate eukaryotic cells, and sequester nutrients. Which T6SS-mediated functions are generalisable across bacteria of a species or are specific to particular strains is little known. Here, we use...

Horizontal gene transfer via plasmids could favour cooperation in bacteria, because transfer of a cooperative gene turns non-cooperative cheats into cooperators. This hypothesis has received support from theoretical, genomic and experimental analyses. By contrast, we show here, with a comparative analysis across 51 diverse species, that genes for e...

Different bird species have completely different parent-offspring interactions. When food is plentiful, the chicks that are begging the loudest are fed the most. When food is scarce, bird species instead feed the largest offspring. While this variation could be due to parents responding to signalling differently based on food availability, it could...

Pathogenic bacteria respond to antibiotic pressure with the evolution of resistance but survival can also depend on their ability to tolerate antibiotic treatment, known as persistence. While a variety of resistance mechanisms and underlying genetics are well characterised in vitro and in vivo , the evolution of persistence, and how it interacts wi...

Individuals are expected to avoid mating with relatives as inbreeding can reduce offspring fitness, a phenomenon known as inbreeding depression. This has led to the widespread assumption that selection will favour individuals that avoid mating with relatives. However, the strength of inbreeding avoidance is variable across species and there are num...

In many species that raise young in cooperative groups, breeders live an exceptionally long time despite high investment in offspring production. How is this possible given the expected trade-off between survival and reproduction? One possibility is that breeders extend their lifespans by outsourcing parental care to non-reproductive group members....

Horizontal gene transfer via plasmids could favour cooperation in bacteria, because transfer of a cooperative gene turns non-cooperative cheats into cooperators. This hypothesis has received support from both theoretical and genomic analyses. In contrast, with a comparative analysis across 51 diverse species, we found that genes for extracellular p...

Since Hamilton published his seminal papers in 1964, our understanding of the importance of cooperation for life on Earth has evolved beyond recognition. Early research was focused on altruism in the social insects, where the problem of cooperation was easy to see. In more recent years, research into cooperation has expanded across the entire tree...

Male-only parental care, while rare in most animals, is a widespread strategy within teleost fish. The costs and benefits to males of acting as sole carer are highly variable among fish species making it challenging to determine the selective pressures driving the evolution of male-only care to such a high prevalence. We conducted a phylogenetic me...

Many bacterial genes encode proteins that are secreted extracellularly. These proteins can be considered cooperative because all surrounding cells can benefit from their production. Therefore, it has been hypothesized that these cooperative genes would more frequently lie on mobile elements, such as plasmids, which can transfer to other cells. This...

Group-living species show a diversity of social organization, from simple mated pairs to complex communities of interdependent individuals performing specialized tasks. The advantages of living in cooperative groups are well understood, but why some species breed in small aggregations while others evolve large, complex groups with clearly divided r...

In birds that breed cooperatively in family groups, adult offspring often delay dispersal to assist the breeding pair in raising their young. Kin selection is thought to play an important role in the evolution of this breeding system. However, evidence supporting the underlying assumption that helpers increase the reproductive success of breeders i...

Inclusive fitness requires a careful accounting of all the fitness effects of a particular behavior. Verbal arguments can potentially exaggerate the inclusive fitness consequences of a behavior by including the fitness of relatives that was not caused by that behavior, leading to error. We show how this “double‐counting” error can arise, with a rec...

The growth and virulence of bacteria depends upon a number of factors that are secreted into the environment. These factors can diffuse away from the producing cells, to be either lost or used by cells that do not produce them (cheats). Mechanisms that act to reduce the loss of secreted factors through diffusion are expected to be favoured. One suc...

A single cheating mutant can lead to the invasion and eventual eradication of cooperation from a population. Consequently, cheat invasion is often considered equal to extinction in empirical and theoretical studies of cooperator-cheat dynamics. But does cheat invasion necessarily equate extinction in nature? By following the social dynamics of iron...

The evolution of helping behaviour in species that breed cooperatively in family groups is typically attributed to kin selection alone. However, in many species, helpers go on to inherit breeding positions in their natal groups, but the extent to which this contributes to selection for helping is unclear as the future reproductive success of helper...

Interview with Ashleigh Griffin, who studies the evolution of cooperative behaviour at the University of Oxford.

A single cheating mutant can lead to the invasion and eventual eradication of cooperation from a population. Consequently, cheat invasion is often considered as 'game over' in empirical and theoretical studies of cooperator-cheat dynamics, especially when cooperation is necessary for fulfilling an essential function. But is cheat invasion necessari...

Type II toxin-antitoxin (TA) systems are most commonly composed of two genes encoding a stable toxin, which harms the cell, and an unstable antitoxin that can inactivate it. TA systems were initially characterized as selfish elements, but have recently gained attention for regulating general stress responses responsible for pathogen virulence, form...

Extended overview of TA diversity. This table adds to Table 1 by including the location in the genome of TA pairs and that of the genomic islands on which they reside, and where these have previously been described. TA names in green show pairs identified by TAfinder but not verified by BLASTP analyses. Conserved domains of TAs found by unrestricte...

Overview of TA prevalence in P. aeruginosa isolates. For each isolate is stated whether it comes from a CF patient or the environment, its clone type, the total number of TA systems (including four core genome pairs), the isolate number (as listed in Marvig et al., 2015b), the clone type's persistence in the patient, whether the clone type had been...

Supporting online material (Data Sheet 1): Alignments for each toxin and antitoxin, with the unique sequence(s) and the reference from TAfinder, denoted as “ref” and by the acquisition number from GenBank. Alignments are followed by the results for conserved domains from an unrestricted BLASTP search, or the top hits from a BLASTP search with Entre...

Estimation of the frequency of loss and gain of GIs with TA pairs in the environment. Some clonetypes found in multiple CF patients had been independently acquired from the environment. We identified the lowest possible number of events of loss or gain of GIs between two isolates of the same clone type as the difference in GIs, and estimated the ti...

Animals living in harsh environments, where temperatures are hot and rainfall is unpredictable, are more likely to breed in cooperative groups. As a result, harsh environmental conditions have been accepted as a key factor explaining the evolution of cooperation. However, this is based on evidence that has not investigated the order of evolutionary...

Indole is a key environmental cue that is used by many organisms. Based on its biochemistry, we suggest indole is used so universally, and by such different organisms, because it derives from the metabolism of tryptophan, a resource essential for many species yet rare in nature. These properties make it a valuable, environmental cue for resources a...

Indole is a key environmental cue that is used by many organisms. Based on its biochemistry, we suggest indole is used so universally, and by such different organisms, because it derives from the metabolism of tryptophan, a resource essential for many species yet rare in nature. These properties make it a valuable, environmental cue for resources a...

The sterile worker castes found in the colonies of social insects are often cited as archetypal examples of altruism in nature. The challenge is to explain why losing the ability to mate has evolved as a superior strategy for transmitting genes into future generations. We propose that two conditions are necessary for the evolution of sterility: com...

Significance Should a chick beg for food even if it isn’t struggling to grow? Does it have anything to lose? The answer could be “yes” if it risks losing indirect fitness through the starvation of siblings. Evolutionary theory suggests that offspring may be more likely to exaggerate signals of need when they compete with less-related nestmates or a...

Cooperation is defined as any adaptation that has evolved, at least in part, to increase the reproductive success of the actor's social partners. Inclusive fitness theory reveals that cooperation can be favoured by natural selection owing to either direct fitness benefits (mutually beneficial cooperation) or indirect fitness benefits (altruistic co...

When competing for space and resources, bacteria produce toxins known as bacteriocins to gain an advantage over competitors. Recent studies in the laboratory have confirmed theoretical predictions that bacteriocin production can determine coexistence, by eradicating sensitive competitors or driving the emergence of resistant genotypes. However, the...

Microbes engage in cooperative behaviours by producing and secreting public goods, the benefits of which are shared among cells, and are therefore susceptible to exploitation by non-producing cheats. In nature, bacteria are not typically colonizing sterile, rich environments in contrast to laboratory experiments, which involve inoculating sterile c...

A nest of begging chicks invites an intuitive explanation: needy chicks want to be fed and parents want to feed them. Surprisingly, however, in a quarter of species studied, parents ignore begging chicks. Furthermore, parents in some species even neglect smaller chicks that beg more, and preferentially feed the biggest chicks that beg less. This ex...

Long life is a typical feature of individuals living in cooperative societies. One explanation is that group living lowers mortality, which selects for longer life. Alternatively, long life may make the evolution of cooperation more likely by ensuring a long breeding tenure, making helping behaviour and queuing for breeding positions worthwhile. Th...

The production of beneficial public goods is common in the microbial world, and so is cheating - the exploitation of public goods by non-producing mutants. Here, we examine co-evolutionary dynamics between cooperators and cheats and ask whether cooperators can evolve strategies to reduce the burden of exploitation, and whether cheats in turn can im...

Bacteriocins are toxins produced by bacteria to kill competitors of the same species. Theory and laboratory experiments suggest that bacteriocin production and immunity play a key role in the competitive dynamics of bacterial strains. The extent to which this is the case in natural populations, especially human pathogens, remains to be tested. We e...

Significance Laboratory experiments show that bacteria have surprisingly complex social lives: Like humans, they can cooperate but also cheat each other. Cooperation could benefit bacteria causing infection by coordinating attack and producing toxins in a collective effort. But can cheaters, exploiting the work of others, affect the outcome of infe...

Animals use signals to coordinate a wide range of behaviours, from feeding offspring to predator avoidance. This poses an evolutionary problem, because individuals could potentially signal dishonestly to coerce others into behaving in ways that benefit the signaller. Theory suggests that honest signalling is favoured when individuals share a common...

Microbial cells rely on cooperative behaviours that can breakdown as a result of exploitation by cheats. Recent work on cheating in microbes, however, has produced examples of populations benefiting from the presence of cheats and/or cooperative behaviours being maintained despite the presence of cheats. These observations have been presented as ev...

Pseudomonas aeruginosa, is an opportunistic, bacterial pathogen causing persistent and frequently fatal infections of the lung in patients with cystic fibrosis. Isolates from chronic infections differ from laboratory and environmental strains in a range of traits and this is widely interpreted as the result of adaptation to the lung environment. Ty...

The term "cheating" is used in the evolutionary and ecological literature to describe a wide range of exploitative or deceitful traits. Although many find this a useful short hand, others have suggested that it implies cognitive intent in a misleading way, and is used inconsistently. We provide a formal justification of the use of the term "cheat"...

Lower visibility of female scientists, compared to male scientists, is a potential reason for the under-representation of women among senior academic ranks. Visibility in the scientific community stems partly from presenting research as an invited speaker at organized meetings. We analysed the sex ratio of presenters at the European Society for Evo...

Supplementary Methods S1.

Variation in the costs of paternal care for male future reproductive success (ZrCost). Colour codings: red, primates; black, birds; blue, fish; green, insects. Bars represent ± 1 SE and the size of the dots is equal to sample size (log(N)). Dashed line is the mean effect size and the grey region is the 95% CI calculated using a Bayesian mixed model...

The correspondence between adjustment of care by males (green), the risk cuckoldry (blue), and the costs of paternal care (red) across the phylogeny of birds. Larger circles represented larger values. Blanks, no data available. (TIF)

Meta-analysis of benefit: methodological effects. (DOCX)

Data used for analysis of rAdjust. (DOCX)

Meta-analysis of cost: methodological effects. (DOCX)

Meta-analysis of adjustment: methodological effects. (DOCX)

Variation in the benefit of paternal care for offspring fitness (effect size = ZrBenefit). Colour codings: red, primates; black, birds; blue, fish; green, insects. Bars represent ± 1 SE and the size of the dots is equal to sample size (log(N)). Dashed line is the mean effect size and the grey region is the 95% CI calculated using a Bayesian mixed m...

Funnel plots for (a) rAdjust, (b) rBenefit, and (c) rCost. Filled circles indicate actual data points and open circles represent potential missing data points identified by the trim and fill analyses. (TIF)

Data used for analysis of rCost. (DOCX)

Data used for analysis of rBenefit. (DOCX)

Phylogenetic meta-analysis of adjustment of paternal care across just birds. (DOCX)

Supplementary results. (DOCX)

Meta-analysis of adjustment: biological effects. (DOCX)

Author Summary In most species where it has been studied, males do not abandon or reduce paternal care when they are cuckolded by other males. These observations have presented a long-standing challenge to our understanding of what drives selection for paternal care. Our analysis of cuckolded fathers from 50 species of birds, fish, mammals, and ins...

Laboratory experiments have shown that the fitness of microorganisms can depend on cooperation between cells. Although this insight has revolutionized our understanding of microbial life, results from artificial microcosms have not been validated in complex natural populations. We investigated the sociality of essential virulence factors (crystal t...

Arising from M. A. Nowak, C. E. Tarnita & E. O. Wilson 466, 1057-1062 (2010); Nowak et al. reply. The paper by Nowak et al. has the evolution of eusociality as its title, but it is mostly about something else. It argues against inclusive fitness theory and offers an alternative modelling approach that is claimed to be more fundamental and general,...

Theory predicts that the evolution of cooperative behaviour is favoured by low levels of promiscuity leading to high within-group relatedness. However, in vertebrates, cooperation often occurs between non-relatives and promiscuity rates are among the highest recorded. Here we resolve this apparent inconsistency with a phylogenetic analysis of 267 b...

Repression of competition (RC) within social groups has been suggested as a key mechanism driving the evolution of cooperation, because it aligns the individual's proximate interest with the interest of the group. Despite its enormous potential for explaining cooperation across all levels of biological organization, ranging from fair meiosis, to po...

There is growing awareness of the importance of cooperative behaviours in microbial communities. Empirical support for this insight comes from experiments using mutant strains, termed 'cheats', which exploit the cooperative behaviour of wild-type strains. However, little detailed work has gone into characterising the competitive dynamics of coopera...

Cooperation is defined as any adaptation that has evolved, at least in part, to increase the reproductive success of the actor's social partners. Inclusive fitness theory reveals that cooperation can be favoured by natural selection owing to either direct fitness benefits (mutually beneficial cooperation) or indirect fitness benefits (altruistic co...

Medical science is typically pitted against the evolutionary forces acting upon infective populations of bacteria. As an alternative strategy, we could exploit our growing understanding of population dynamics of social traits in bacteria to help treat bacterial disease. In particular, population dynamics of social traits could be exploited to intro...

Hamilton demonstrated that the evolution of cooperative behaviour is favoured by high relatedness, which can arise through kin discrimination or limited dispersal (population viscosity). These two processes are likely to operate with limited overlap: kin discrimination is beneficial when variation in relatedness is higher, whereas limited dispersal...

There has been extensive theoretical debate over whether population viscosity (limited dispersal) can favour cooperation. While limited dispersal increases the probability of interactions occurring between relatives, which can favour cooperation, it can also lead to an increase in competition between relatives and this can reduce or completely nega...

Although cooperative systems can persist in nature despite the potential for exploitation by noncooperators, it is often observed that small changes in population demography can tip the balance of selective forces for or against cooperation. Here we consider the role of population density in the context of microbial cooperation. First, we account f...

There is strong evidence that natural selection can favour phenotypic plasticity as a mechanism to maximize fitness in animals. Here, we aim to investigate phenotypic plasticity of a cooperative trait in bacteria--the production of an iron-scavenging molecule (pyoverdin) by Pseudomonas aeruginosa. Pyoverdin production is metabolically costly to the...

The ability of pathogenic bacteria to exploit their hosts depends upon various virulence factors, released in response to the concentration of small autoinducer molecules that are also released by the bacteria [1-5]. In vitro experiments suggest that autoinducer molecules are signals used to coordinate cooperative behaviors and that this process of...

Numerous theoretical studies have investigated how limited dispersal may provide an explanation for the evolution of cooperation, by leading to interactions between relatives. However, despite considerable theoretical attention, there has been a lack of empirical tests. In this article, we test how patterns of dispersal influence the evolution of c...

The term quorum sensing (QS) is used to describe communication between bacterial cells, whereby a coordinated population response is controlled by diffusible signal molecules. QS has not only been described between cells of the same species (intraspecies), but also between bacterial species (interspecies) and between bacteria and higher organisms (...

In our social semantics review (J. Evol. Biol., 2007, 415–432), we discussed some of the misconceptions and sources of confusion associated with group selection. Wilson (2007, this issue) claims that we made three errors regarding group selection. Here, we aim to expand upon the relevant points from our review in order to refute this claim. The las...

Our understanding of the social lives of microbes has been revolutionized over the past 20 years. It used to be assumed that bacteria and other microorganisms lived relatively independent unicellular lives, without the cooperative behaviors that have provoked so much interest in mammals, birds, and insects. However, a rapidly expanding body of rese...

It has been suggested that bacterial cells communicate by releasing and sensing small diffusible signal molecules in a process commonly known as quorum sensing (QS). It is generally assumed that QS is used to coordinate cooperative behaviours at the population level. However, evolutionary theory predicts that individuals who communicate and coopera...

In the cooperatively breeding superb fairy-wren, helpers have negligible effect on breeding success. So why help? The answer is hidden in the size of the eggs.

Why should organisms cooperate with each other? Helping close relatives that are likely to share the same genes (kin selection) is one important explanation that is likely to apply across taxa. The production of metabolically costly extracellular iron-scavenging molecules (siderophores) by microorganisms is a cooperative behaviour because it benefi...

Hamilton's inclusive fitness theory provides a leading explanation for the problem of cooperation. A general result from inclusive fitness theory is that, except under restrictive conditions, cooperation should not be subject to frequency-dependent selection. However, several recent studies in microbial systems have demonstrated that the relative f...

Hamilton’s inclusive fitness theory provides a leading explanation for the problem of cooperation. A general result from inclusive fitness theory is that, except under restrictive conditions, cooperation should not be subject to frequency‐dependent selection. However, several recent studies in microbial systems have demonstrated that the relative f...

Natural selection favours genes that increase an organism's ability to survive and reproduce. This would appear to lead to a world dominated by selfish behaviour. However, cooperation can be found at all levels of biological organisation: genes cooperate in genomes, organelles cooperate to form eukaryotic cells, cells cooperate to make multicellula...

Appendix. (0.53 MB PDF)

Lack of competition for food items in banded mongoose litters allows pups to benefit from more demanding siblings, suggesting that in this species begging may not be entirely selfish.

From an evolutionary perspective, social behaviours are those which have fitness consequences for both the individual that performs the behaviour, and another individual. Over the last 43 years, a huge theoretical and empirical literature has developed on this topic. However, progress is often hindered by poor communication between scientists, with...

The term quorum sensing (QS) is used to describe the communication between bacterial cells, whereby a coordinated population response is controlled by diffusible molecules produced by individuals. QS has not only been described between cells of the same species (intraspecies), but also between species (interspecies) and between bacteria and higher...

The ability of bacteria to evolve resistance to antibiotics has been much reported in recent years. It is less well-known that within populations of bacteria there are cells which are resistant due to a non-inherited phenotypic switch to a slow-growing state. Although such 'persister' cells are receiving increasing attention, the evolutionary force...