Late-life fitness gains and reproductive death in Cardiocondyla obscurior ants

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    Evaluation Summary:

    Evolution of ageing remains only partially understood, and this research will be of interest to evolutionary biologists, entomologists, or anyone intrigued by senescence. The authors focus on following a large number of ant (C. obscurior) colonies and provide intriguing data in relation to age-specific mortality and reproduction. The gist of their argument is that the mortality is decreasing with age while reproduction (production of sexuals) is increasing with age, such that there is little evidence of ageing in this species. The experimental design is elegant and the data collection thorough, providing insight into the rarely observed final stages of an ant colonies life. The analyses are mostly sound, but the conclusions would benefit from a broader exploration of the structure and constraints inherent to ant societies.

    (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. The reviewers remained anonymous to the authors.)

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Abstract

A key hypothesis for the occurrence of senescence is the decrease in selection strength due to the decrease in the proportion of newborns from parents attaining an advanced age – the so-called selection shadow. Strikingly, queens of social insects have long lifespans and reproductive senescence seems to be negligible. By lifelong tracking of 99 Cardiocondyla obscurior (Formicidae: Myrmicinae) ant colonies, we find that queens shift to the production of sexuals in late life regardless of their absolute lifespan or the number of workers present. Furthermore, RNAseq analyses of old queens past their peak of reproductive performance showed the development of massive pathology while queens were still fertile, leading to rapid death. We conclude that the evolution of superorganismality is accompanied by ‘continuusparity,’ a life history strategy that is distinct from other iteroparous and semelparous strategies across the tree of life, in that it combines continuous reproduction with a fitness peak late in life.

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  1. Author Response:

    Reviewer #1 (Public Review):

    This is an interesting study looking at the evolution of ageing in social insects using ants as a model. As I haven't seen the initial submission, I have looked at the manuscript and the response to reviewers and I base my suggestions on both documents.

    Evolution of ageing remains only partially understood and this field seems to be experiencing a sort of renaissance in recent years with a surge of theoretical advances and new empirical findings. Queens of social insects, and ant queens in particular, have remarkable lifespans and understanding the biology of their long life can help in understanding the biology of ageing in a more general sense.

    In this study, the authors focus on following quite a large number of ant (C. obscurior) colonies and provide intriguing data in relation to age-specific mortality and reproduction. The gist of their argument is that the mortality is decreasing with age while reproduction (production of sexuals) is increasing with age, such that there is little evidence of ageing in this species.

    Overall I think this is an interesting dataset that provides important information that will advance the field. However, I think the manuscript currently lacks clarity, structure and suffers from poor formulation of ideas in places, and is rather difficult to follow even for an expert in the field. I think that it requires quite a bit of work to sort this out. However, I also have a methodological question (#15) which could be key for the interpretation of the results.

    We hope that this manuscript is clearer now, especially with the additional data.

    My understanding is that queens live for 40-50 weeks max (Fig. S3). Fig. 4 suggests that from week 30 onwards the production of eggs, worker pupae and queen pupae decline. This suggests that while queen mortality declines in late life, so does queen reproduction. So, do queens of this species show reproductive senescence?

    Yes, they do experience reproductive senescence.

    The data do suggest that relative investment into reproduction (queen worker ratio) increases with age, but the absolute number of queens declines with age. This suggests an interesting result from the life-history theory perspective - increased investment in reproduction with reduced residual reproductive value, but not necessarily the absence of reproductive senescence. Please clarify.

    We hope this new version of the manuscript addresses clearly that ants queens do experience reproductive senescence and actuarial senescence, but only after late in life (after the peak of sexual investment is reached). Therefore, we state that senescence is delayed.

    Reviewer #2 (Public Review):

    The authors investigated the evolutionary drivers of delayed senescence in ant queens by carefully observing the survival and productivity of C. obscurior colonies that were maintained at 10, 20, or 30 workers. They show that the 10 worker treatment produces fewer new queens, and lower quality workers, indicating low colony efficiency under a reduced workforce. The authors focused their conclusions on the observation of a hump-shaped relative mortality curve, with queens having a higher than average mortality around 30 weeks and then a lower than expected mortality around 40 weeks. The colonies produced more queens at the end of their lifespan, so the authors conclude high fitness gains at the end of life selects for minimal senescence in ant queens, thus generating the drop in mortality they observed at 40 weeks.

    There is a large body of research focused on the early life stage and establishment of ant colonies, but relatively little that follows their worker and reproductive trajectory to the end of life. Partially, this is because many commonly studied ant species have a lifespan too long to feasibly track, and partially because most ant species do not readily produce sexual queens or males in the lab setting. For this alone, the study provides valuable insight into the ant lifecycle and demonstrates that C. obscurior is an ideal species for future study. The experimental design and analyses are sound, and I must acknowledge the incredible amount of work that must have gone into the data collection. However, I have some serious concerns about how the results are interpreted, and what is left out of the discussion on ant colony structure and limitations that are crucial to reaching accurate conclusions.

    One issue is that the conclusions hinge on the observation that relative queen mortality decreases at the latest observational period, around 40 weeks. The authors raise this as evidence that queens are under selection for reduced senescence, as they also conclude that fitness gains (queen production) are highest late in life. The problem is that according to figure S3, only a handful of queens survive past week 40, and they all manage to hang on for another month or two before dying out. I cannot be sure how many colonies survive to this period from how the data is presented, but I worry that the authors are resting their conclusion on a low number of particularly tenacious queens. These colony numbers should be provided, and the authors should demonstrate that the drop in mortality is observable even if these outliers are excluded.

    Fitness gains are highest late in life, and this is shown for all queens, regardless whether they are short- or long-lived. Therefore, selection is maintained until late in life. We calculate relative mortality as a function of age as in Jones et al. (2014), (Fig. 4.) As suggested by the first reviewer we also now include age-specific mortality of the best-model fitted using BaSTA and the estimated parameters in the supplement (Figure 4 - Figure supplement 1, Supplementary File 8 and 9). We have also included RNAseq data of queens near and middle-aged queens. The data support our conclusion of a delayed selection shadow, as age signs were not obvious in the middle-aged queens. This is in line with two studies (Wyschetzki et al. MBE 2015; Harrison GBE et al. 2021), where no signs of aging were found in middle-aged queens of the same species.

    It also appears that the queen pupae production drops off precipitously during the end of the observational period, according to figure 4A, which runs counter to the argument that selection is reducing senescence in these older queens because they have high reproductive output at this stage. The authors put a lot of emphasis on the queen/worker ratio being highest at the end of the observational period, but this doesn't necessarily mean queens are receiving the highest fitness during this period. A queen would have a high queen to worker production ratio if she lays one worker and one queen, but she would have higher fitness if she lays 100 workers and 10 queens. Figure 2A indicates that the highest overall queen pupae laying occurs around 30 weeks, which actually corresponds with the highest level of relative queen mortality. The question of fitness gains at advanced queen age would be better answered by just analyzing which stage in their life they produced the most queen pupae. Does the queen laying rate reach a maximum and remain stable for the rest of a queen's life, or does it decrease along with worker production as they reach end of life? Figure 4A makes it appear that it decreases towards end of life, but I'm not sure if that is only because so few colonies lasted until the end of the observational period.

    We have included that “This caste ratio shift does not occur because a drop of pupae production at the end of life. Actually, pupae production is at its highest just before death (Figure 2 - Figure supplement 1).” We added a figure with raw numbers of pupae produced at the end of life for the 99 tracked queens.

    Another factor that should be discussed is sperm depletion. The authors state that each queen mated with a single male when they set up the colonies, so sperm depletion may be more important than senescence for determining the reproductive lifespan of these queens. I'm not sure if this species is normally single mated in the wild, or the length of their natural colony lifespan, but this is important information to provide in order to dismiss issues of sperm depletion in this study. Without this information it is impossible to determine if the decrease in egg laying towards the end of the study is due to senescence or sperm depletion.

    Taken together, it could be argued that these data better support selection on an optimal lifespan, around 30 weeks, as opposed to selection for directional extended lifespan and reduced senescence. If the reproductive benefits of an extended lifespan are capped by sperm depletion, the alternative strategy would be to produce a robust workforce as quickly and efficiently as possible, and then produce as many sexual offspring as possible with the remaining sperm. Perhaps selection has determined that the optimal length of this cycle is around 30 weeks, with variation dependent on the amount of sperm transferred during mating and the condition of the queen. This possibility should be addressed, and if possible additional data should be provided on sperm depletion in C. obscurior, and the colonies that survived to the end of the observation period. Without these additions, the conclusions on senescence and lifespan remain tenuous.

    We now discuss in the manuscript that sperm depletion is not commonly seen in this species, and also occurred only once in this study (of the 99 colonies). All colonies were tracked until death. Therefore, there is no evidence of stabilizing selection to a lifespan of 30 weeks based on sperm depletion. This manuscript addresses the question of how is the “shape” of aging in this species, and not the “pace” (lifespan extension), but gives a hint on why extended lifespans should be favored.

  2. Evaluation Summary:

    Evolution of ageing remains only partially understood, and this research will be of interest to evolutionary biologists, entomologists, or anyone intrigued by senescence. The authors focus on following a large number of ant (C. obscurior) colonies and provide intriguing data in relation to age-specific mortality and reproduction. The gist of their argument is that the mortality is decreasing with age while reproduction (production of sexuals) is increasing with age, such that there is little evidence of ageing in this species. The experimental design is elegant and the data collection thorough, providing insight into the rarely observed final stages of an ant colonies life. The analyses are mostly sound, but the conclusions would benefit from a broader exploration of the structure and constraints inherent to ant societies.

    (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. The reviewers remained anonymous to the authors.)

  3. Reviewer #1 (Public Review):

    This is an interesting study looking at the evolution of ageing in social insects using ants as a model. As I haven't seen the initial submission, I have looked at the manuscript and the response to reviewers and I base my suggestions on both documents.

    Evolution of ageing remains only partially understood and this field seems to be experiencing a sort of renaissance in recent years with a surge of theoretical advances and new empirical findings. Queens of social insects, and ant queens in particular, have remarkable lifespans and understanding the biology of their long life can help in understanding the biology of ageing in a more general sense.

    In this study, the authors focus on following quite a large number of ant (C. obscurior) colonies and provide intriguing data in relation to age-specific mortality and reproduction. The gist of their argument is that the mortality is decreasing with age while reproduction (production of sexuals) is increasing with age, such that there is little evidence of ageing in this species.

    Overall I think this is an interesting dataset that provides important information that will advance the field. However, I think the manuscript currently lacks clarity, structure and suffers from poor formulation of ideas in places, and is rather difficult to follow even for an expert in the field. I think that it requires quite a bit of work to sort this out. However, I also have a methodological question (#15) which could be key for the interpretation of the results.

    My understanding is that queens live for 40-50 weeks max (Fig. S3). Fig. 4 suggests that from week 30 onwards the production of eggs, worker pupae and queen pupae decline. This suggests that while queen mortality declines in late life, so does queen reproduction. So, do queens of this species show reproductive senescence?

    The data do suggest that relative investment into reproduction (queen worker ratio) increases with age, but the absolute number of queens declines with age. This suggests an interesting result from the life-history theory perspective - increased investment in reproduction with reduced residual reproductive value, but not necessarily the absence of reproductive senescence. Please clarify.

  4. Reviewer #2 (Public Review):

    The authors investigated the evolutionary drivers of delayed senescence in ant queens by carefully observing the survival and productivity of C. obscurior colonies that were maintained at 10, 20, or 30 workers. They show that the 10 worker treatment produces fewer new queens, and lower quality workers, indicating low colony efficiency under a reduced workforce. The authors focused their conclusions on the observation of a hump-shaped relative mortality curve, with queens having a higher than average mortality around 30 weeks and then a lower than expected mortality around 40 weeks. The colonies produced more queens at the end of their lifespan, so the authors conclude high fitness gains at the end of life selects for minimal senescence in ant queens, thus generating the drop in mortality they observed at 40 weeks.

    There is a large body of research focused on the early life stage and establishment of ant colonies, but relatively little that follows their worker and reproductive trajectory to the end of life. Partially, this is because many commonly studied ant species have a lifespan too long to feasibly track, and partially because most ant species do not readily produce sexual queens or males in the lab setting. For this alone, the study provides valuable insight into the ant lifecycle and demonstrates that C. obscurior is an ideal species for future study. The experimental design and analyses are sound, and I must acknowledge the incredible amount of work that must have gone into the data collection. However, I have some serious concerns about how the results are interpreted, and what is left out of the discussion on ant colony structure and limitations that are crucial to reaching accurate conclusions.

    One issue is that the conclusions hinge on the observation that relative queen mortality decreases at the latest observational period, around 40 weeks. The authors raise this as evidence that queens are under selection for reduced senescence, as they also conclude that fitness gains (queen production) are highest late in life. The problem is that according to figure S3, only a handful of queens survive past week 40, and they all manage to hang on for another month or two before dying out. I cannot be sure how many colonies survive to this period from how the data is presented, but I worry that the authors are resting their conclusion on a low number of particularly tenacious queens. These colony numbers should be provided, and the authors should demonstrate that the drop in mortality is observable even if these outliers are excluded.

    It also appears that the queen pupae production drops off precipitously during the end of the observational period, according to figure 4A, which runs counter to the argument that selection is reducing senescence in these older queens because they have high reproductive output at this stage. The authors put a lot of emphasis on the queen/worker ratio being highest at the end of the observational period, but this doesn't necessarily mean queens are receiving the highest fitness during this period. A queen would have a high queen to worker production ratio if she lays one worker and one queen, but she would have higher fitness if she lays 100 workers and 10 queens. Figure 2A indicates that the highest overall queen pupae laying occurs around 30 weeks, which actually corresponds with the highest level of relative queen mortality. The question of fitness gains at advanced queen age would be better answered by just analyzing which stage in their life they produced the most queen pupae. Does the queen laying rate reach a maximum and remain stable for the rest of a queen's life, or does it decrease along with worker production as they reach end of life? Figure 4A makes it appear that it decreases towards end of life, but I'm not sure if that is only because so few colonies lasted until the end of the observational period.

    Another factor that should be discussed is sperm depletion. The authors state that each queen mated with a single male when they set up the colonies, so sperm depletion may be more important than senescence for determining the reproductive lifespan of these queens. I'm not sure if this species is normally single mated in the wild, or the length of their natural colony lifespan, but this is important information to provide in order to dismiss issues of sperm depletion in this study. Without this information it is impossible to determine if the decrease in egg laying towards the end of the study is due to senescence or sperm depletion.

    Taken together, it could be argued that these data better support selection on an optimal lifespan, around 30 weeks, as opposed to selection for directional extended lifespan and reduced senescence. If the reproductive benefits of an extended lifespan are capped by sperm depletion, the alternative strategy would be to produce a robust workforce as quickly and efficiently as possible, and then produce as many sexual offspring as possible with the remaining sperm. Perhaps selection has determined that the optimal length of this cycle is around 30 weeks, with variation dependent on the amount of sperm transferred during mating and the condition of the queen. This possibility should be addressed, and if possible additional data should be provided on sperm depletion in C. obscurior, and the colonies that survived to the end of the observation period. Without these additions, the conclusions on senescence and lifespan remain tenuous.