Arnaud Pocheville

Inheritance is where physiology meets evolution

Physiology and evolutionary biology have developed as two separated disciplines, a separation that mirrored the hypothesis that the physiological and evolutionary processes could be decoupled. We argue that non‐genetic inheritance shatters the frontier between physiology and evolution, and leads to the coupling of physiological and evolutionary processes to a point where there exists a continuum between accommodation by phenotypic plasticity and adaptation by natural selection. This approach is also profoundly affecting the definition of the concept of phenotypic plasticity, which should now be envisaged as a multi‐scale concept. We further suggest that inclusive inheritance provides a quantitative way to help bridging infra‐individual (i.e. physiology) with supra‐individual (i.e. evolution) approaches, in a way that should help building the long sough inclusive evolutionary synthesis.

Measuring Causal Specificity

Several authors have argued that causes differ in the degree to which they are ‘specific’ to their effects. Woodward has used this idea to enrich his influential interventionist theory of causal explanation. Here we propose a way to measure causal specificity using tools from information theory. We show that the specificity of a causal variable is not well defined without a probability distribution over the states of that variable. We demonstrate the tractability and interest of our proposed measure by measuring the specificity of coding DNA and other factors in a simple model of the production of mRNA.

From bottom-up approaches to levels of organization and extended critical transitions

Biological thinking is structured by the notion of level of organization. We will show that this notion acquires a precise meaning in critical phenomena: they disrupt, by the appearance of infinite quantities, the mathematical (possibly equational) determination at a given level, when moving at an “higher” one. As a result, their analysis cannot be called genuinely bottom-up, even though it remains upward in a restricted sense. At the same time, criticality and related phenomena are very common in biology. Because of this, we claim that bottom-up approaches are not sufficient, in principle, to capture biological phenomena. In the second part of this paper, following (Bailly, 1991b), we discuss a strong criterium of level transition. The core idea of the criterium is to start from the breaking of the symmetries and determination at a “first” level in order to “move” at the others. If biological phenomena have multiple, sustained levels of organization in this sense, then they should be interpreted as extended critical transitions.

Theoretical principles for biology: Variation

Darwin introduced the concept that random variation generates new living forms. In this paper, we elaborate on Darwins notion of random variation to propose that biological variation should be given the status of a fundamental theoretical principle in biology. We state that biological objects such as organisms are specific objects. Specific objects are special in that they are qualitatively different from each other. They can undergo unpredictable qualitative changes, some of which are not defined before they happen. We express the principle of variation in terms of symmetry changes, where symmetries underlie the theoretical determination of the object. We contrast the biological situation with the physical situation, where objects are generic (that is, different objects can be assumed to be identical) and evolve in well-defined state spaces. We derive several implications of the principle of variation, in particular, biological objects show randomness, historicity and contextuality. We elaborate on the articulation between this principle and the two other principles proposed in this special issue: the principle of default state and the principle of organization.

The Ecological Niche: History and Recent Controversies

In this chapter, we first trace the history of the concept of ecological niche and see how its meanings varied with the search for a theory of ecology. The niche concept has its roots in the Darwinian view of ecosystems that are structured by the struggle for survival and, originally, the niche was perceived as an invariant place within the ecosystem, that would preexist the assembly of the ecosystem. The concept then slipped towards a sense in which the niche, no longer a pre-existing ecosystem structure, eventually became a variable that would in turn have to be explained by the competitive exclusion principle and the coevolution of species. This concept, while more operational from an empirical point of view than the previous one, suffered from an ill-founded definition. A recent refoundation by Chase & Leibold enabled to overcome some of the definitional difficulties.

Reverse-engineering the genetic circuitry of a cancer cell with predicted intervention in chronic lymphocytic leukemia

Cellular behavior is sustained by genetic programs that are progressively disrupted in pathological conditions—notably, cancer. High-throughput gene expression profiling has been used to infer statistical models describing these cellular programs, and development is now needed to guide orientated modulation of these systems. Here we develop a regression-based model to reverse-engineer a temporal genetic program, based on relevant patterns of gene expression after cell stimulation. This method integrates the temporal dimension of biological rewiring of genetic programs and enables the prediction of the effect of targeted gene disruption at the system level. We tested the performance accuracy of this model on synthetic data before reverse-engineering the response of primary cancer cells to a proliferative (protumorigenic) stimulation in a multistate leukemia biological model (i.e., chronic lymphocytic leukemia). To validate the ability of our method to predict the effects of gene modulation on the global program, we performed an intervention experiment on a targeted gene. Comparison of the predicted and observed gene expression changes demonstrates the possibility of predicting the effects of a perturbation in a gene regulatory network, a first step toward an orientated intervention in a cancer cell genetic program.

Drosophila mate copying correlates with atmospheric pressure in a speed learning situation

Mate choice can strongly affect fitness in sexually reproducing organisms. A form of mate choice is mate copying, in which individuals use information about potential mates by copying the mate choice of other individuals. While many studies have documented mate copying, little is known about the effect of environmental conditions on this behaviour. Here, we report the first evidence that Drosophila melanogaster females can acquire a sexual preference for one male characteristic after witnessing a single mate choice event (i.e. speed learning). We also found that mate copying was correlated with air pressure and air pressure changes, so that females copied far more when air pressure was high and increasing, i.e. in good and improving weather conditions. These results reveal a quick social observational learning and highlight the potential importance of meteorological conditions for mate copying, a trait potentially driving reproductive isolation.

Toward a theory of organisms: Three founding principles in search of a useful integration

Organisms, be they uni- or multi-cellular, are agents capable of creating their own norms; they are continuously harmonizing their ability to create novelty and stability, that is, they combine plasticity with robustness. Here we articulate the three principles for a theory of organisms, namely: the default state of proliferation with variation and motility, the principle of variation and the principle of organization. These principles profoundly change both biological observables and their determination with respect to the theoretical framework of physical theories. This radical change opens up the possibility of anchoring mathematical modeling in biologically proper principles.

Workers agonistic interactions in queenright and queenless nests of a polydomous ant society

In eusocial Hymenoptera, the ability of workers to reproduce is a cause of conflict, both between the queen and workers and among workers. Reproductive decisions by workers depend on parameters such as colony size (which reduces the cost of selfish reproduction for the colony) or queen fertility. Indeed, queen signals inhibit reproduction from workers either by coercion or because of self-restraint. Multinest societies called polydomous facilitate the collection of scattered food and colony movement in an unstable environment. In these societies, queen signal dispersion could be hindered by the physical absence of queen in some nests. Here we investigate how polydomy influences worker behaviour in a monogynous polydomous ant, the ponerinae Pachycondyla goeldii. A recent field study has shown that P. goeldii workers display a significantly higher ovarian development in secondary (queenless) than in primary (queenright) nests. In the present study we show that P. goeldii workers change they behaviour when they colonize new nests, displaying significantly more agonistic behaviours in secondary than in primary nests. Behavioural changes and ovary development of workers from secondary nests are probably because of a decrease of queen signal intensity in their nests. The rise of agonistic behaviour in these nests stems from mechanisms regulating the reproduction of workers such as policing or hierarchy set-up. Our results lead us to favour the hypothesis of hierarchy establishment between workers in the secondary nests, which characterize large colonies. Pachycondyla goeldii colonies therefore maximize their reproductive output by triggering worker reproduction when colony size increases.

Physiology and evolution at the crossroads of plasticity and inheritance

In Danchin & Pocheville (2014), we urged that physiology and evolution be better integrated, as it is more and more apparent that they represent two facets of a single biological process. The first reason for this integration is somehow classical but still essential. Physiology is central in determining the selective value of organisms, and thus the evolutionary dynamics. Physiology itself can evolve, for instance towards local physiological optima. In providing a physical model to explain the inverse relationship between heart rate and body size in mammals, Lin Wang & Wang (2015) exemplify such an integration of physiology and evolution. The second reason to better integrate these two processes is that physiology is now more and more widely recognized as a direct cause of hereditary variation. For evolutionary theory, such an impact of physiology is a striking novelty. Indeed, hereditary variation serves as a fuel for natural selection and has usually been assumed to be ‘blind’ to the physiology of organisms, a hypothesis often framed in terms of ‘random’ mutation (Pocheville & Danchin, in press). Epigenetic mechanisms seem to have a central role in linking physiology and evolution, as they are at the same time mechanisms of plasticity and non-genetic inheritance, and mechanisms which favour genetic mutation. The momentum recently gained by the study of epigenetic mechanisms brings physiology back at the heart of evolution.