Tradeoff breaking as a model of evolutionary transitions in individuality and limits of the fitness-decoupling metaphor
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Evaluation Summary:
Key steps in the evolution of more complex life involve evolutionary transitions in individuality-the origin of new biological entities (i.e., multicellular organisms). This paper presents a novel criterion for measuring when this transition has occurred, via the presence of trade-off breaking adaptations. This work has considerable merit and will be of particular interest for diverse researchers studying transitions in individuality. Some of the author's overarching claims require further clarification.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1, Reviewer #2 and Reviewer #3 agreed to share their names with the authors.)
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Abstract
Evolutionary transitions in individuality (ETIs) involve the formation of Darwinian collectives from Darwinian particles. The transition from cells to multicellular life is a prime example. During an ETI, collectives become units of selection in their own right. However, the underlying processes are poorly understood. One observation used to identify the completion of an ETI is an increase in collective-level performance accompanied by a decrease in particle-level performance, for example measured by growth rate. This seemingly counterintuitive dynamic has been referred to as fitness decoupling and has been used to interpret both models and experimental data. Extending and unifying results from the literature, we show that fitness of particles and collectives can never decouple because calculations of fitness performed over appropriate and equivalent time intervals are necessarily the same provided the population reaches a stable collective size distribution. By way of solution, we draw attention to the value of mechanistic approaches that emphasise traits, and tradeoffs among traits, as opposed to fitness. This trait-based approach is sufficient to capture dynamics that underpin evolutionary transitions. In addition, drawing upon both experimental and theoretical studies, we show that while early stages of transitions might often involve tradeoffs among particle traits, later—and critical—stages are likely to involve the rupture of such tradeoffs. Thus, when observed in the context of ETIs, tradeoff-breaking events stand as a useful marker of these transitions.
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Author Response:
Reviewer #1:
Significance: A central puzzle in evolutionary biology (and philosophy of biology) is the evolution of new (collective) entities that can evolve on their own right (e.g. the evolution of multicellular organisms from single cells). These evolutionary transitions are often conceptualized in terms of fitness decoupling (a fitness increase of the collective even as the fitness of the component particles decreases). Using a life-history model, the authors show that fitness decoupling is not possible when the conditions for fitness are the same. Thus, this paper has the potential to change how we think about the evolution of new collective entities.
Strengths: This paper is conceptually rich and the overall argument is clear. Re-analyzing previous data/models using their new framework highlights new patterns …
Author Response:
Reviewer #1:
Significance: A central puzzle in evolutionary biology (and philosophy of biology) is the evolution of new (collective) entities that can evolve on their own right (e.g. the evolution of multicellular organisms from single cells). These evolutionary transitions are often conceptualized in terms of fitness decoupling (a fitness increase of the collective even as the fitness of the component particles decreases). Using a life-history model, the authors show that fitness decoupling is not possible when the conditions for fitness are the same. Thus, this paper has the potential to change how we think about the evolution of new collective entities.
Strengths: This paper is conceptually rich and the overall argument is clear. Re-analyzing previous data/models using their new framework highlights new patterns of fitness change in these transitions of individuality, and as such, it provides novel and exciting avenues of research.
Weaknesses: While the overall argument is clear, some of the details can be hard to follow (even as someone familiar with the literature). The initial description of their model is fairly clear, but given its conceptual novelty, the paper does not spend enough time developing the different concepts of fitness at the particle level.
Moreover, it is not entirely clear what is at stake: what is the role of fitness decoupling in our understanding of fitness transitions? And how does the proposed mechanistic ("trade-off breaking") model serve as a replacement? It seems to me like trade-off breaking is a characteristic of many evolutionary innovations, not only of major transitions. It seems even possible to envision groups that allow for an escape in a trade-off without leading to the evolution of a new "Darwinian" individual.
For example, one could conceive of a trade-off in zebras between time spent foraging and protection against predators. Coming together temporarily as a group is likely to allow for values outside this trade-off space (similar to those in Fig. 6). One could even imagine a new mutation that makes zebras switch activities (foraging/watching) depending on their position within the group. This mutation is only available to zebras that form groups (the phenotype does not exist in the absence of a group). But I would still want to argue that there is more to the evolution of new levels of individuality. Trade-off breaking seems (potentially) a necessary, but not sufficient step in these transitions.
And while the language of the authors is careful to not suggest sufficiency, it is not entirely clear how this approach helps us understand the particularity of these transitions.
Reviewer #1 asks first to clarify the stakes: what is the role of fitness decoupling in the explanation and how does tradeoff-breaking replace or supplement it? Second, they requested us to make a statement about the necessary or sufficient nature of tradeoff-breaking.
With respect to the second point, we argue that tradeoff breaking is not sufficient, but is probably necessary for an ETI to occur.
Let us now clarify the role of fitness decoupling and tradeoff breaking in the explanation of ETIs. It must be stressed that tradeoff breaking does not “replace” fitness decoupling; rather, tradeoff breaking is an event that cannot be understood readily in the framework of fitness decoupling. Thus, we claim that ETIs are better understood when seen through the lenses of traits and the evolutionary constraints that link them (i.e., tradeoffs) than via the export-of-fitness model (i.e., fitness decoupling). To illustrate this, we use the zebra herd example proposed by the reviewer. Coming together temporarily as a collective does not, in itself, constitute a tradeoff-breaking event, but rather simply a collective-formation event (similar to the first ace2 mutation in snowflake yeast or the first WS mutation in the Pseudomonas system). From this starting point, a number of mutations (i.e., change in traits values) can be fixed in the population that improve the performance of zebras within this environment. This is the “fast” part of the evolutionary trajectory that occurs on the ancestral tradeoff, which we called “low hanging fruit mutations” in the manuscript. As a consequence, “optimal herds within the ancestral tradeoff” evolve. As stated in the manuscript, if we assume that the tradeoff on traits is identical for lone zebra and zebra herd and also assume that the ancestral lone zebra exhibit trait values that are optimal (within these constraints) for lone zebras, it follows that the low-hanging fruit mutations that improve the zebra herd will probably reduce counterfactual fitness. This lowering of counterfactual fitness is not due to a “transfer” between real and counterfactual fitness (because there is nothing to transfer between real and counterfactual worlds), but is a consequence of the differential contribution of the traits involved in the tradeoff to the two fitness quantities. However, this specificity of the tradeoff might be significant because it could lead to stabilisation of the new collectives through ratchetting.
There is, indeed, “more to the evolution of new levels of individuality,” as pointed out by Reviewer #1. We claim that it involves rare mutations that would overcome the ancestral constraint and call them “tradeoff breaking mutations”. Tradeoff-breaking mutations are not bound by ancestral tradeoff; therefore, there is no a priori theoretical or biological reason to think they would have any positive or negative effect on counterfactual fitness. Here, we must stop using the zebra herd example because no tradeoff-breaking mutation occurred. However, the tradeoff-breaking lineages in the Pseudomonas example exhibit an improvement of both counterfactual and within-collective fitness. This observation does not fit within an export-of-fitness framework, but makes perfect sense in a traits-based view of ETIs—as a tradeoff-breaking mutation.
Reviewer #2:
This work reviews the influential "fitness decoupling" heuristic for understanding evolutionary transitions in individuality (ETIs), describes some of its limitations, and clarifies its interpretation. The review of the fitness decoupling account capably describes an interpretation of this framework that has frequently occurred in the literature, for example in Okasha 2006, Godfrey-Smith 2011, Hammerschmidt et al. 2014, Black et al. 2019, and Rose et al. 2020. However, it does not address the interpretation advanced by its authors, Richard Michod and colleagues, which they have clarified in several papers cited in the present work. Michod and colleagues have argued that the fitness decoupling account describes a changing relationship between the fitness of groups and the "counterfactual" fitness of their component cells, that is, the fitness the cells would have if they were removed from the group. This point is made explicitly in Shelton & Michod 2104 and Shelton & Michod 2020 and was present (though perhaps not as obvious) in Michod 2005 and later works, in contrast to the claim in the Glossary that this is a "relatively recent development of the fitness decoupling literature." The interpretation that Michod embraces is similar to what is here described as f2, the fitness of a "theoretical mono-particle collective", but that interpretation is not mentioned in the present work until Section 2.3. It is possible that an argument could be made that Michod and colleagues have not consistently interpreted fitness decoupling this way, or have made statements inconsistent with this interpretation, but no such argument is present in this work. Thus the impression conveyed is that Michod and colleagues consider decoupling of "commensurably computed fitnesses" possible, which is counter to their explicit statements on the topic.
The description of the limitations of the fitness decoupling heuristic (Section 2) is useful and goes a considerable distance toward clarifying the ways in which fitness decoupling can rigorously be interpreted. However, the final assessment (Section 2.3) does not make a compelling case for its central argument, the lack of utility of the fitness decoupling concept. Elsewhere in the work, the ratcheting model of Libby and colleagues is referenced in comparison to the tradeoff-breaking approach, but Section 2.3 does not acknowledge the relationship between Libby and colleagues' model and the counterfactual interpretation of the fitness decoupling heuristic. For example, the argument in Libby and Ratcliff 2014 that "If any of the yeast that evolved high rates of apoptosis within clusters were to leave the group and revert to a unicellular lifestyle, they would find themselves at a competitive disadvantage relative to other, low-apoptosis unicellular strains." and in Libby et al. 2016 that "…if G cells were to revert to unicellular I cells, they would be quickly outcompeted" are counterfactual fitness arguments essentially similar to that of Shelton and Michod 2020 that "the fitness a cell would have on its own declines as the transition progresses." Section 2 makes a convincing case that commensurable fitnesses cannot be decoupled, but by fixating on commensurability, which is not relevant to the counterfactual interpretation of fitness decoupling, Section 2.4 fails to make a convincing case that "fitness-decoupling observations do little to clarify the process of an ETI." That is, "because they are not commensurable" does little to explain why the counterfactual interpretation of fitness decoupling "does little on its own to clarify the process of an ETI," since commensurability is not a claim that the the counterfactual interpretation of fitness decoupling makes.
We agree with the reviewer on two essential points: (1) the decoupling of commensurably computed fitness is impossible when collectives have a finite size and (2) counterfactual fitness is not commensurable to particle or collective fitness.
While we recognise that Michod and collaborators did clarify that fitness decoupling referred to counterfactual fitness (although, to us, this becomes clear from 2015 onward), we argue that the fitness transfer (or export-of-fitness) metaphor implies (by its wording) a commensurability of fitnesses that undermine this welcome clarification.
Indeed, for a quantity to be transferred from one place—or component—to another, the source and destination must be commensurable. It is incorrect to talk about a transfer between counterfactual and actual quantities. A better choice of words to discuss the relative change of counterfactual and actual quantities would avoid the physical transfer metaphor and focus instead on the correlation of the two quantities. It must be noted that, despite the clarification of counterfactual fitness, the word “transfer” continues to be used in recent work (Davison & Michod, 2021).
This may seem like nitpicking; however, there is a real advantage in being careful about this. We do agree that, under some assumptions, counterfactual fitness would decrease while whole–life cycle particle fitness (or collective fitness) increases. From there, one might ask: what needs explaining? If one assumes an export-of-fitness framework, the transfer of fitness explains why it cannot be otherwise. If fitness decreases on one side, it must increase on the other. In other words, the existence of a tradeoff is taken for granted based on the improper physical metaphor. While there are strong reasons to think that such tradeoffs exist, they should be assessed in their own right and on a case-by-case basis rather than being assumed to hold. Otherwise, there is no way to make sense of the tradeoff-breaking scenario described in Section 4.
By the same token, the metaphor of “decoupling” often associated with the export-of-fitness model is misleading because it is used to describe a part of the evolutionary dynamics where counterfactual particle fitness and whole–life cycle particle fitness are strongly dependant on one another (even if their changes are anticorrelated), through the existence of the tradeoff.
Nevertheless, we welcome the reviewer’s urge to clarify our position and how this relates to Michod and colleagues’ counterfactual fitness proposal.
The model based on trade-offs and trade-off breaking is useful and likely to be of interest to theorists interested in ETIs. The observation that this model can reproduce the (counterfactual) fitness-decoupling observation is a useful in showing the how the two models relate. The result that counterfactual fitness decoupling is a consequence rather than a cause of the evolutionary dynamics is an important point (though perhaps obvious in retrospect, since counterfactuals, things to do not happen, can't be the causes of anything).
The caution in Section 3.3 that "the same [counterfactual fitness decoupling] observation will be made in any situation in which short-term costs are compensated by long-term benefits, not solely during ETIs" is a good point, and it sets up the argument that trade-off breaking is a "genuine marker for an ETI". However, no convincing case is made that the same criticism, that the observed phenomenon is not unique to ETIs, is not equally true of trade-off breaking. Some nice examples of trade-off breaking in the context of ETIs are given, but these do not amount to an argument that trade-off breaking is only observed during ETIs. The life history literature includes examples of trade-off breaking that are not related to ETIs, so it is not clear that trade-off breaking is either a reliable indicator of ETIs or superior in this respect to counterfactual fitness decoupling.
This point is in line with one of the points made by Reviewer #1. We have now clarified our position with respect to the generality of the tradeoff-breaking approach.
In the Discussion, the "inconveniences" associated with the fitness decoupling are cogent limitations of this heuristic. The "impossibility of decoupling between commensurable measures of fitness" is an important result, but it is not new and should thus probably not be presented as "[o]ur first main finding". Shelton and Michod 2014 includes a mathematical proof in the appendix that, given the model assumptions, "consideration of the births and deaths of colonies gives us exactly the same bottom line (fitness) as consideration of the births and deaths of lone cells." The second main finding, that "fitness decoupling observations cannot be reliably used as a marker for ETIs," is valid, but as described above, a convincing case is not made that trade-off breaking can be reliably used in this manner, either. Trade-off breaking may, however, be a useful way to think about ETIs in the other ways that are suggested, for example as key events and as stepping stones to new hypotheses.
We have now clarified our position.
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Evaluation Summary:
Key steps in the evolution of more complex life involve evolutionary transitions in individuality-the origin of new biological entities (i.e., multicellular organisms). This paper presents a novel criterion for measuring when this transition has occurred, via the presence of trade-off breaking adaptations. This work has considerable merit and will be of particular interest for diverse researchers studying transitions in individuality. Some of the author's overarching claims require further clarification.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1, Reviewer #2 and Reviewer #3 agreed to share their names with the authors.)
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Reviewer #1 (Public Review):
Significance: A central puzzle in evolutionary biology (and philosophy of biology) is the evolution of new (collective) entities that can evolve on their own right (e.g. the evolution of multicellular organisms from single cells). These evolutionary transitions are often conceptualized in terms of fitness decoupling (a fitness increase of the collective even as the fitness of the component particles decreases). Using a life-history model, the authors show that fitness decoupling is not possible when the conditions for fitness are the same. Thus, this paper has the potential to change how we think about the evolution of new collective entities.
Strengths: This paper is conceptually rich and the overall argument is clear. Re-analyzing previous data/models using their new framework highlights new patterns of …
Reviewer #1 (Public Review):
Significance: A central puzzle in evolutionary biology (and philosophy of biology) is the evolution of new (collective) entities that can evolve on their own right (e.g. the evolution of multicellular organisms from single cells). These evolutionary transitions are often conceptualized in terms of fitness decoupling (a fitness increase of the collective even as the fitness of the component particles decreases). Using a life-history model, the authors show that fitness decoupling is not possible when the conditions for fitness are the same. Thus, this paper has the potential to change how we think about the evolution of new collective entities.
Strengths: This paper is conceptually rich and the overall argument is clear. Re-analyzing previous data/models using their new framework highlights new patterns of fitness change in these transitions of individuality, and as such, it provides novel and exciting avenues of research.
Weaknesses: While the overall argument is clear, some of the details can be hard to follow (even as someone familiar with the literature). The initial description of their model is fairly clear, but given its conceptual novelty, the paper does not spend enough time developing the different concepts of fitness at the particle level.
Moreover, it is not entirely clear what is at stake: what is the role of fitness decoupling in our understanding of fitness transitions? And how does the proposed mechanistic ("trade-off breaking") model serve as a replacement? It seems to me like trade-off breaking is a characteristic of many evolutionary innovations, not only of major transitions. It seems even possible to envision groups that allow for an escape in a trade-off without leading to the evolution of a new "Darwinian" individual.
For example, one could conceive of a trade-off in zebras between time spent foraging and protection against predators. Coming together temporarily as a group is likely to allow for values outside this trade-off space (similar to those in Fig. 6). One could even imagine a new mutation that makes zebras switch activities (foraging/watching) depending on their position within the group. This mutation is only available to zebras that form groups (the phenotype does not exist in the absence of a group). But I would still want to argue that there is more to the evolution of new levels of individuality. Trade-off breaking seems (potentially) a necessary, but not sufficient step in these transitions.
And while the language of the authors is careful to not suggest sufficiency, it is not entirely clear how this approach helps us understand the particularity of these transitions.
-
Reviewer #2 (Public Review):
This work reviews the influential "fitness decoupling" heuristic for understanding evolutionary transitions in individuality (ETIs), describes some of its limitations, and clarifies its interpretation. The review of the fitness decoupling account capably describes an interpretation of this framework that has frequently occurred in the literature, for example in Okasha 2006, Godfrey-Smith 2011, Hammerschmidt et al. 2014, Black et al. 2019, and Rose et al. 2020. However, it does not address the interpretation advanced by its authors, Richard Michod and colleagues, which they have clarified in several papers cited in the present work. Michod and colleagues have argued that the fitness decoupling account describes a changing relationship between the fitness of groups and the "counterfactual" fitness of their …
Reviewer #2 (Public Review):
This work reviews the influential "fitness decoupling" heuristic for understanding evolutionary transitions in individuality (ETIs), describes some of its limitations, and clarifies its interpretation. The review of the fitness decoupling account capably describes an interpretation of this framework that has frequently occurred in the literature, for example in Okasha 2006, Godfrey-Smith 2011, Hammerschmidt et al. 2014, Black et al. 2019, and Rose et al. 2020. However, it does not address the interpretation advanced by its authors, Richard Michod and colleagues, which they have clarified in several papers cited in the present work. Michod and colleagues have argued that the fitness decoupling account describes a changing relationship between the fitness of groups and the "counterfactual" fitness of their component cells, that is, the fitness the cells would have if they were removed from the group. This point is made explicitly in Shelton & Michod 2104 and Shelton & Michod 2020 and was present (though perhaps not as obvious) in Michod 2005 and later works, in contrast to the claim in the Glossary that this is a "relatively recent development of the fitness decoupling literature." The interpretation that Michod embraces is similar to what is here described as f2, the fitness of a "theoretical mono-particle collective", but that interpretation is not mentioned in the present work until Section 2.3. It is possible that an argument could be made that Michod and colleagues have not consistently interpreted fitness decoupling this way, or have made statements inconsistent with this interpretation, but no such argument is present in this work. Thus the impression conveyed is that Michod and colleagues consider decoupling of "commensurably computed fitnesses" possible, which is counter to their explicit statements on the topic.
The description of the limitations of the fitness decoupling heuristic (Section 2) is useful and goes a considerable distance toward clarifying the ways in which fitness decoupling can rigorously be interpreted. However, the final assessment (Section 2.3) does not make a compelling case for its central argument, the lack of utility of the fitness decoupling concept. Elsewhere in the work, the ratcheting model of Libby and colleagues is referenced in comparison to the tradeoff-breaking approach, but Section 2.3 does not acknowledge the relationship between Libby and colleagues' model and the counterfactual interpretation of the fitness decoupling heuristic. For example, the argument in Libby and Ratcliff 2014 that "If any of the yeast that evolved high rates of apoptosis within clusters were to leave the group and revert to a unicellular lifestyle, they would find themselves at a competitive disadvantage relative to other, low-apoptosis unicellular strains." and in Libby et al. 2016 that "...if G cells were to revert to unicellular I cells, they would be quickly outcompeted" are counterfactual fitness arguments essentially similar to that of Shelton and Michod 2020 that "the fitness a cell would have on its own declines as the transition progresses." Section 2 makes a convincing case that commensurable fitnesses cannot be decoupled, but by fixating on commensurability, which is not relevant to the counterfactual interpretation of fitness decoupling, Section 2.4 fails to make a convincing case that "fitness-decoupling observations do little to clarify the process of an ETI." That is, "because they are not commensurable" does little to explain why the counterfactual interpretation of fitness decoupling "does little on its own to clarify the process of an ETI," since commensurability is not a claim that the the counterfactual interpretation of fitness decoupling makes.
The model based on trade-offs and trade-off breaking is useful and likely to be of interest to theorists interested in ETIs. The observation that this model can reproduce the (counterfactual) fitness-decoupling observation is a useful in showing the how the two models relate. The result that counterfactual fitness decoupling is a consequence rather than a cause of the evolutionary dynamics is an important point (though perhaps obvious in retrospect, since counterfactuals, things to do not happen, can't be the causes of anything).
The caution in Section 3.3 that "the same [counterfactual fitness decoupling] observation will be made in any situation in which short-term costs are compensated by long-term benefits, not solely during ETIs" is a good point, and it sets up the argument that trade-off breaking is a "genuine marker for an ETI". However, no convincing case is made that the same criticism, that the observed phenomenon is not unique to ETIs, is not equally true of trade-off breaking. Some nice examples of trade-off breaking in the context of ETIs are given, but these do not amount to an argument that trade-off breaking is only observed during ETIs. The life history literature includes examples of trade-off breaking that are not related to ETIs, so it is not clear that trade-off breaking is either a reliable indicator of ETIs or superior in this respect to counterfactual fitness decoupling.
In the Discussion, the "inconveniences" associated with the fitness decoupling are cogent limitations of this heuristic. The "impossibility of decoupling between commensurable measures of fitness" is an important result, but it is not new and should thus probably not be presented as "[o]ur first main finding". Shelton and Michod 2014 includes a mathematical proof in the appendix that, given the model assumptions, "consideration of the births and deaths of colonies gives us exactly the same bottom line (fitness) as consideration of the births and deaths of lone cells." The second main finding, that "fitness decoupling observations cannot be reliably used as a marker for ETIs," is valid, but as described above, a convincing case is not made that trade-off breaking can be reliably used in this manner, either. Trade-off breaking may, however, be a useful way to think about ETIs in the other ways that are suggested, for example as key events and as stepping stones to new hypotheses.
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Reviewer #3 (Public Review):
Bourrat et al take on the idea of fitness decoupling in evolutionary transitions in individuality; using theoretical approaches and some available empirical data, they question the meaningfulness of fitness decoupling and suggest instead an alternative framework that looks at rare mutations that break tradeoffs between the lower and the higher level, e.g., a tradeoff between growth at the lower level vs survival or dispersal at the higher level. This is an important question and worthwhile endeavor, useful in guiding not only theoretical investigations but also empirical measurements.
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