Project
Association Theory
Initial Question
Why do organisms recognize kin?
When I entered graduate school in 2003, it was thought that kin recognition evolves in response to "cheaters" that fail to act altruistically. In social amoebae, such cheaters would be those that avoided producing sterile stalk and only produced fertile spores. My first goal was to isolate cheater mutants from a natural population. I would then show, in the laboratory, how they select for kin recognition. After searching for cheaters in a natural population of Dictyostelium discoideum, however, I found none (Figs. 1 and 2). Yet, I found that D. discoideum can potentially recognize kin (Fig. 3).
Fig. 1. Photographs of Dictyostelium discoideum fruiting body formation following dung collections. (A) Culmination of wild amoebae in situ on dung into a slug. (B) Fruiting of wild fruiting body on dung. (C) Fruiting body formation on dead fly hatched from dung. (D) Fruiting body on dead maggot hatched from dung.
Fig. 2. Photographs of clonal isolations on hay infusion agar at 64 hours. (A) Wild clone. (B) AX4 fbxA–. (C) Wild clone close-up. (D) AX4 fbxA– close-up. Nothing that resembled AX4 fbxA– was found among natural isolates.
Fig. 3. I found evidence of discriminatory segregation in D. discoideum, suggestive of kin recognition. (A) I found two fruiting bodies each composed of a single clone, found together near salamander feces under a rock. (B) Fruiting bodied contained clone S2-1 and S2-3. (C) S2-1 and S2-3 were mixed at equal ratios, and allowed to fruit on a sterilized deer pellet or agar. (D) On the deer pellet, uniclonal fruiting bodies of either genotype were found. Contrary to prior studies, this suggested discriminatory segregation in D. discoideum. I shared these findings in a lab meeting on Sep. 12, 2005.
Approach
Repeating the same mix experiment as in Fig. 3D with other pairs of clones, however, I found immediately that other pairs clones that naturally co-occur do not segregate strongly. I later showed this more extensively (Gilbert et al. 2012). At the time, around 2006, I transitioned my research to focus on how that kin recognition evolves. A paper by Rousset and Roze (2007) questioned the idea that kin recognition evolves in response to cheaters.
association Theory
In 2009, I first submitted a paper describing a new model of kin recognition, which I also shared at a conference. My model distinguished differential treatment (help/harm) and association preference (differentially entering the contexts for interactions). My model suggested that kin recognition could evolve for the purpose of association preference in response to differential treatment. I eventually published this model in 2015, after developing it for specific application to marine invertebrates (following a discussion with Andrew Murray from Harvard, who suggested to me that new ideas are best understood when applied to a particular biological situation).
Predictions
Separate cues
Kin recognition involves a perception component and a cue component, and can evolve adaptively by modification of either component. They key feature is the extreme genetic polymorphism of the cue, which ensures that allelic variants are unlikely to be shared with non-kin.
My model showed that a requirement for the adaptive evolution of polymorphism is that separate cues are used for association preference (segregation or rejection) as for differential treatment (harm or help). My model also showed that the use of separate cues could itself be selectively favored.
Evidence suggests that separate cues are used in bacteria, protochordates, cnidarians, fungi, plasmodial slime molds, arthropods, and vertebrates. I therefore predict that this may be true also in social amoebae, at least in species that segregate strongly.
association Preference
In addition to explaining kin recognition, my model yielded new predictions for the evolution of kin association preference. Previously, it was thought that organisms associate preferentially with kin in order to direct help to kin. However, some non-cooperative organisms, like frog tadpoles and fish, associate preferentially with kin. My model showed that such kin association preference can evolve in response to discriminatory harming behaviors. This provided an explanation for association preference behaviors in both cooperative and non-cooperative species. It extends to cooperative species because harming behaviors are often prevalent as behaviors that rob benefits of cooperation.
Implications for social theory
Hamilton's rule
My model revealed that social theorists had long confused fundamental types of social behavior. For example, evolutionists had applied Hamilton's rule for altruism to association. When testing Hamilton's rule, moreover, they treated the lifetime reproductive success (LRS) of a solitary individual as baseline. This led to frequent violations of Hamilton's rule. In contrast, my theoretical framework, which I called "association theory," restricts Hamilton's rule to social actions. It suggests that to measure the b and c terms of Hamilton's rule correctly, it is important to treat the LRS of an associated individual as baseline. In a pair of articles, I show that this can prevent violations of Hamilton's rule and yield new predictions for the adaptive basis of behavior.
Major transitions
Social theorists have split major transitions in biological individuality into three key steps: the origin, maintenance, and transformation of social groups. Typically, they downplay the importance of kin discrimination in major transitions. Incorporating the evolution of differential treatment and association preference into a theory of evolutionary transitions, however, suggest that they often involve the following steps: the the origin of association (aggregation or fusion), the evolution of differential treatment, the evolution of association preference, a switch in cues, and the evolution of kin recognition.
Inclusive fitness
Inclusive-fitness theory states that a positive inclusive-fitness effect is the universal criterion for a trait or behavior to be favored by selection. Because the inclusive-fitness effect is defined as rb - c, this states that Hamilton's rule rb - c > 0 is a general explanation for any behavior or trait. In a recent article, I showed that restricting Hamilton's rule to social actions can prevent apparent violations of Hamilton's rule and lead to reinterpretations of empirical studies.
discrepancy to prevalent research
A number of authors have given the impression that D. discoideum segregates strongly. However, this is because they cherry-pick clones that segregate strongly for their experiments. Gilbert et al. (2012) focused on an unbiased sample of naturally co-occurring clones.
Returning social theory to Darwinian foundations
To determine why a complex trait evolved, it is important to break them into simpler components and ask how the sub-component traits interact and became integrated into a complex whole. My work suggests that predictive power can be gained by a stepwise historical model for diverse taxa.
Project
Natural Reward Theory
Initial Question
How might we extend Darwinism to explain macroevolution?
The theory of natural selection does not predict a tendency towards progress in evolution. This was emphasized by Haldane, then Fisher, and then Wright. In social evolution, natural selection can just as easily favor selfish behaviors that reduce mean fitness, as it can favor cooperative behaviors that increase mean fitness. Natural selection can also cause organisms to become highly adapted to some narrow way of life, leaving them vulnerable to extinction with changes of environment. Therefore, natural selection does not inherently produce traits that predispose organisms to colonization of new environments. It can just as easily produce a duck-billed platypus as a human.
Approach
Reexamining core assumptions
I had learned from my textbooks that Darwin had defined the conditions for natural selection as (1) variation, (2) inheritance, and (3) differential reproductive success (or differential "fitness"). Thus, it seemed that natural selection might apply to any level that can reproduce ("has fitness"). Because species can seemingly reproduce with speciation and die with extinction, it seemed that natural selection might apply to the species level.
If natural selection applies to the species level, then why did Darwin focus on within-species competition?
The Struggle for existence
Darwin mentioned "the struggle for existence" as a requirement for natural selection. Contained in the "struggle for existence" was the idea that populations are limited by various "checks to increase." These could include those imposed by resource limitations, like food and water. However, they could also include limits on population growth imposed by predators and parasites. As a consequence of this assumption, only types within species would have the potential to competitively displace each other. Different species, experiencing different checks to increase, would have the potential to coexist.
Most evolutionists thought that Darwin's focus on death, competition, and "struggle" appealed to fashions of the day. It harkened Malthusian competition and Tennyson's "nature red in tooth and claw." Authors like Fisher, Dobzhansky, and Lewontin derided Darwin's metaphor. It was thus largely excised from the philosophical structure of evolutionary theory.
I realized, however, that Darwin's metaphor defined the levels of competition relevant to natural selection. The key to extending Darwin's theory was to allow for a different type of evolutionary struggle.
the Struggle for supremacy
Under the struggle for supremacy, the first forms to escape checks to increase expand in population, diversify, and are protected from invasion by competitors. Thus, the incumbent advantage of being first to innovate is the reward for innovation in nature. It is also a primary source of constraint. Through the dual processes of invention-conquest macroevolution and extinction-replacement megaevolution, however, natural reward can over time advance life by increasing its innovative capacity. Reading the literature, I found that the form of competition in macroevolution was not direct Darwinian competition as usually assumed, but instead usually required that an incumbent dwindle or go extinct before being replaced. This was consistent with the idea of an "incumbent advantage" and the notion of a "struggle for supremacy." Darwin himself used the term "struggle for supremacy" only in an unpublished manuscript, and usually used the term "struggle to produce new and modified descendants."
natural reward
One day for convenience, I used "natural reward" to delineate the benefit of the incumbent advantage. I soon realized that "natural reward" was not a placeholder term, but reflected a second non-random force of evolution. In 2020, I outlined the theory of natural reward.
the success of the innovative
The theory of natural reward suggests that the broad-scale history of life is not "the survival of the fittest" but "the success of the innovative." This makes sense because "fitness" is best defined as a narrow concept, relevant to the choice between alternative alleles within a species. Natural selection acting on genotypes results in the survival of the fittest alleles. Thus, natural selection typically proceeds as allele frequency change. When selective values are frequency dependent, or when average effects of alleles are not constant, mean fitness can decrease. In contrast, natural reward favors only those inventions that allow spreading into new environments, which means that natural reward is inherently progressive (expansive).
Practical implications
The theory of natural reward suggests that there is progress in evolution, that man is set apart his innovative capacity, and that evolutionary theory provides a guide for human ethics. It suggest that the history of life is summarized as "the success of the innovative," and that nature rewards the most cooperative, creative, adaptable, and entrepreneurial forms of life. The theory of natural reward suggests that science progresses in explanatory power and ability to resolve anomalies. It suggests that innovation by one group of people can benefit others. It suggests that things are "good" that promote truth-seeking, cooperation, creativity, meritocracy, and prosperity, and "evil" those things that promote corruption, selfishness, conformity, nihilism, and poverty. The theory of natural reward also suggests that with innovation come creative destruction, such that a compassionate stance is to limit the negative effects of creative destruction by lifting up those who are displaced. In that sense, the theory of natural reward provides a subtle approach to human ethics. It also has practical implications for making science more innovative.
Project
Advancing science
Initial Question
Approach
How to get risky ideas funded?
Let's say that through your normal line of research, you have noticed various anomalies, and you can see that these anomalies may be resolved by taking a different approach. You might even accumulate some evidence for your new perspective from existing lines of research. However, because you have not yet had time to develop your theory for applications to many different realms, it is unclear how generally that it applies. In contrast, the existing paradigm has a suite of specialized and diversified models, each claiming to explain some particularly narrow phenomenon. Although these models are marked by various anomalies, most people dismiss them with ad hoc modifications of theory. To develop your new perspective, you must therefore show how that a new theory resolves anomalies and why it yields a synthesis that does not require so many modifications. Moreover, the most powerful way to convince others of your new perspective is to use it as a guide for hypothetico-deductive research. But how can you get your idea funded, especially if it seems threatening to the status quo?
A solution
The economic system of science is structured like a command economy. New lines of research are reviewed by "program officers" who consult experts for reviews, analogous to the bureaucrats of command economies, who direct funding for R&D. As is well known to economists studying the historical difference between the Soviet and American economies, the command structure is risk-averse and fails to innovate in the long term. This is why, for example, the Soviet Union could not match the innovative capacity of the USA over time. In my paper, I have pointed out how to import the capitalistic solution to a situation in which the goods produced are non-appropriable, as in science. I have devised a plan for such a system that could be set up in a Web 3.0 ecosystem. I am currently revising a manuscript that proposes this funding system for science.
Impact
Thanks to an initial query by a military official who read my "natural reward" article, I was motivated to write up my ideas for science funding. After over a year of work, the resulting manuscript was circulated to high-up officials in the US Pentagon and I gave a zoom talk. I am still working on getting this article published, which has been difficult because it has several new ideas.