The geometry of gametic dispersal in a flying mammal, Rhinolophus hipposideros

  1. Thomas Brazier
  2. Diane Zarzoso-Lacoste
  3. Lisa Lehnen
  4. Pierre-Loup Jan
  5. Sebastien J. Puechmaille
  6. Eric J. Petit

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Abstract

Dispersal influences population and evolutionary dynamics, with effects that depend on the dispersal strategies through which gene flow occurs. In some species, mating partners move exclusively for mating, dispersing genes but not individuals. This is the case in many bat species, of which the lesser horseshoe bat ( Rhinolophus hipposideros ) shows a genetic structure at a fine spatial scale suggesting restricted dispersal. We investigated how natal and mating dispersal shape gene flow in this species in two metapopulations using paternity and population assignments. Half of the inferred paternities were intra-colonial and gave an estimate of the mean mating dispersal distance of around 11 km, explaining the observed genetic structure. Complete gametic dispersal distances were further estimated by combining natal with mating dispersal distances. The resulting gametic dispersal kernels showed a mean distance of around 20 km and a fat-tailed distribution typical of an excess of long-distance dispersal movements. It is the first time that natal and mating dispersal distances have been separately estimated and then combined in animals, documenting quantitatively how mating dispersal decorrelates gene and individual flows. It is important to consider this mechanism to explain dispersal evolution.

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  1. Peer Community in Evolutionary Biology

    Dear authors,

    First of all, I would like to apologize for the delay in the review process. Unfortunately, we encountered some difficulties in finding suitable reviewers.

    However, in the end we found two excellent reviewers whose comments you can find attached to this message. As you can see from their feedback, both reviewers found your work valuable. However, they raised some points that should be considered in the revised version of the manuscript. In particular, Reviewer 2 highlights some methodological issues that need clarification and suggests additional analyses to ensure that the interpretations of the results are solid. These are valid points that should be addressed.

    All the best, Marjo Saastamoinen

  2. Peer Community in Evolutionary Biology

    Reviewer comments on:

    The geometry of gametic dispersal in a flying mammal, Rhinolophus hipposideros

    Thomas Brazier, Diane Zarzoso-Lacoste, Lisa Lehnen, Pierre-Loup Jan, Sebastien J. Puechmaille, Eric J. Petit

    https://doi.org/10.1101/2024.10.24.620000, version 1

     

    This interesting and well-executed study by Brazier and colleagues demonstrates how the use of molecular methods can allow assessing for the contribution of otherwise hard-to-detect, short mating dispersal movements to gene flow. The authors use parentage assignment and population assignment to estimate both the natal dispersal distances and mating dispersal distances in two metapopulations of the lesser horseshoe bat (Rhinolophus hipposideros), then combining these to produce an estimate of the complete gametic dispersal kernel in each metapopulation. Disentangling the contributions of these two types of dispersal was enabled by extensive sampling, combined with exceptionally strong genetic differentiation at the spatial scales of only tens of kilometers, allowing the assignment of identified fathers to their colonies of origin. The authors found that both natal and mating dispersal shape the gametic dispersal kernel in the lesser horseshoe bat, and that the combined gametic dispersal kernels fit a fat-tailed distribution, typical for species that are mostly philopatric with some long-distance dispersal events. This is concluded to lead to dispersal-limitation and explain the strong fine-scale population structure within the metapopulations. However, this conclusion would benefit from a more detailed explanation and connections to population genetic theory, as the estimated gametic dispersal distances and therefore gene flow still seem substantial considering the amount of isolation by distance among the colonies.

     

    Title and abstract


    Does the title clearly reflect the content of the article? [X] Yes, [ ] No (please explain), [ ] I don't know

    Does the abstract present the main findings of the study? [X] Yes, [ ] No (please explain), [ ] I don’t know


    Introduction


    Are the research questions/hypotheses/predictions clearly presented? [X] Yes, [ ] No (please explain), [ ] I don’t know

    Does the introduction build on relevant research in the field? [ ] Yes, [ ] No (please explain), [X] I don’t know

    - While the introduction is concise and covers the general background relevant for the study questions, the concept of breeding dispersal (i.e. dispersal between consecutive breedings) and the associated, large body of literature (e.g. Dale et al. 2005; Paradis et al. 1998, Fandos et al. 2023) has not been mentioned. Even if breeding dispersal is not a phenomenon in the lesser horseshoe bat, I would recommend introducing the concept in the introduction to:

    (a) clarify the comprehensiveness of only focusing on natal and mating dispersal to fulfil the aim of the study (estimating the complete gametic dispersal kernel). Give references to why breeding dispersal can be ignored in this species?

    (b) place the study in the context of what we already know (and on the other hand, what we cannot know) based on the earlier work combining natal and breeding dispersal kernels. This would be especially important since the authors make the claim that it is the first time that natal and mating dispersal distances have been separately estimated and then combined in animals - what is the main difference to the previously separately estimated and combined natal and breeding dispersal distances? How are breeding dispersal and mating dispersal conceptually different (e.g. flow of gametes vs. flow of individuals, at least temporally for one breeding season)? Incorporating this should further clarify the novelty of this work in comparison to the existing body of literature on natal & breeding dispersal.

     

    Materials and methods


    Are the methods and analyses sufficiently detailed to allow replication by other researchers? [X] Yes, [ ] No (please explain), [ ] I don’t know

    Are the methods and statistical analyses appropriate and well described? [X] Yes, [ ] No (please explain), [ ] I don’t know

    - The sampling design and sample sizes are in line with what has previously been suggested to produce accurate dispersal kernel estimates using genetic parentage analyses (Bode et al. 2017).

    - While I am not an expert on parentage assignment methods and therefore cannot comment on the technical details of the specific analyses, it is clear that the authors have been exceptionally rigorous in explaining and validating their methods to reduce bias and distinguish observed patterns from potential artefacts. This includes comparisons between empirical and simulated data for hypothesis-testing and the estimation of error rates, applying bootstrap procedures to estimate confidence intervals, and cross-validating results using different, independent approaches. The analysis steps and reasoning are clear and explained in sufficient detail for replication.

     

    Results


    In the case of negative results, is there a statistical power analysis (or an adequate Bayesian analysis or equivalence testing)? [X] Yes, [ ] No (please explain), [ ] I don’t know

    Are the results described and interpreted correctly? [X] Yes, [ ] No (please explain), [ ] I don’t know

    - However, see comment on elaborating when drawing conclusions about the observed dispersal-limitation as an explanation to the pattern of genetic differentiation under the next section

     

    Discussion


    Have the authors appropriately emphasized the strengths and limitations of their study/theory/methods/argument? [X] Yes, [ ] No (please explain), [ ] I don’t know


    Are the conclusions adequately supported by the results (without overstating the implications of the findings)? [ ] Yes, [ ] No (please explain), [X] I don’t know


    - The conclusions are mainly well-supported by the results

    - However, I struggled making the connection to how the estimated dispersal kernel would explain the strong genetic structure in this species (e.g. line 326: “Our results should be relevant to a finer comprehension of why species with apparent sex-biased dispersal show nevertheless genetic structure at a fine scale.”, and line 333: “We observed that variations in individuals mating behaviour shape a skewed dispersal kernel while promoting fine-scale genetic structure”). It seems striking that there is such a clear pattern of isolation-by-distance over just 25 km in both metapopulations, considering that the estimated mean gametic dispersal distance is around 20 km in both (17.6 km and 22.2 km). It could benefit a broader readership if this could be discussed in the context of the population genetic theory regarding the persistence of genetic differentiation under considerable gene flow.

    - In the introduction, it was mentioned that one of the metapopulations is expanding and one is stable. However, I did not notice that this difference would have been revisited in the discussion. Although any statistical comparisons obviously cannot be performed, the differences in the shape of the inferred dispersal kernels could be very briefly discussed in this context.

    - The last sentence of the Conclusions paragraph makes a statement about genetic diversity, even though genetic diversity was not measured in this study and is also not part of the introduction and the framing of this paper.

     

    Review references:

    Bode, M., Williamson, D. H., Harrison, H. B., Outram, N., & Jones, G. P. (2018). Estimating dispersal kernels using genetic parentage data. Methods in Ecology and Evolution, 9(3), 490-501.

    Dale, S., Lunde, A., & Steifetten, Ø. (2005). Longer breeding dispersal than natal dispersal in the ortolan bunting. Behavioral Ecology, 16(1), 20-24.

    Fandos, G., Talluto, L., Fiedler, W., Robinson, R. A., Thorup, K., & Zurell, D. (2023). Standardised empirical dispersal kernels emphasise the pervasiveness of long‐distance dispersal in European birds. Journal of Animal Ecology, 92(1), 158-170.

    Paradis, E., Baillie, S. R., Sutherland, W. J., & Gregory, R. D. (1998). Patterns of natal and breeding dispersal in birds. Journal of Animal ecology, 67(4), 518-536.

     

    Comments by line:

    22: Would remove the first part of the sentence “As individuals move outside their natal site, dispersal is involved in range expansion and colonizations, --" -> Already stated before and not well connected with the rest of the sentence

    38: Although I see what you aim for here, natal dispersal is also not always a permanent movement of an individual (can be followed by breeding dispersal events).

    50: This one-sentence paragraph describing the study aim feels out of place here, recommend combining with the last paragraph of the introduction

    53: Consider changing “interesting species” to e.g. “well-suited/ideal study species” -> if using “interesting”, please also describe from what perspective. Now the following text mentions that it is similar in the characteristics of interest to many other bat species. To me, what makes the species stand out as an ideal study species for this question is its exceptionally strong population structure at that allows making the genetic assignments at such a small scale. I would include it in this paragraph and focus the final paragraph on the aims and hypotheses of your study.

    75: Include the full species name in the first paragraph of Methods: lesser horseshoe à lesser horseshoe bat

    165: “minimal” -> minimum, “maximal” -> maximum

    228: Since it’s just one previous study that you are mentioning, could specify the species

    239: In addition to plant studies, the bird literature is relevant here. Many species exhibit relatively strong philopatry with some long-distance dispersal events, fitting a fat-tailed distribution.

    260 & 263: Combine or rearrange these two one-sentence paragraphs?

    286: “phylopatric” -> philopatric

    293: A somewhat circular conclusion: if the low number of recovered paternities is likely to be due to potential fathers not residing (and therefore not being sampled) within the colonies, how is this mitigated by stating that “Potential fathers are thus more likely to be among colonial fathers”?

    333: “individuals” -> individuals’

     

     

  3. Peer Community in Evolutionary Biology

    Title and abstract
    Does the title clearly reflect the content of the article? 
    Yes
    Does the abstract present the main findings of the study?
    Yes
    Introduction
    Are the research questions/hypotheses/predictions clearly presented? I don’t know
    Yes
    Does the introduction build on relevant research in the field? 
    Yes
    Materials and methods
    Are the methods and analyses sufficiently detailed to allow replication by other researchers? 
    Yes
    Are the methods and statistical analyses appropriate and well described? 
    No. Please see comments 1, 3 and 4
    Results
    In the case of negative results, is there a statistical power analysis (or an adequate Bayesian analysis or equivalence testing)? 
    Yes
    Are the results described and interpreted correctly? 
    Yes
    Discussion
    Have the authors appropriately emphasized the strengths and limitations of their study/theory/methods/argument? 
    No, please see comments 5, 6, and 7
    Are the conclusions adequately supported by the results (without overstating the implications of the findings)? 
    No, please see comment 4

     


    This manuscript examines parentage and population assignments of individuals gleaned from faecal samples. The research is interesting, and is the first to explore gametic dispersal in animals. The manuscript is well written, with clear and useful description of the theory. My main issue with this manuscript is that there is not enough evidence presented to support the findings. The first four comments address this, the latter are related to further discussion points. I look forward to seeing the revised manuscript.

    1.        It appears that the data were collected over multiple years and locations. Please provide evidence that the microsatellite sequencing was calibrated to avoid batch effects. It would also be useful to include how missing data was handled.

    2.        It would be useful to provide additional information on the data to give the audience a better overall picture. Please provide information on microsatellite length, variability and allelic richness.

    3.        To support the assumption of genetically distinct populations, there should be some evidence of metapopulation structure included in this manuscripts, i.e. individual-based PCA and admixture. STRUCTURE should be run a priori, without expectations of population groupings, so structure can be seen.

    4.        Following on from Comment 3, evidence of an a priori run of structure is necessary to demonstrate the separation of colonies that is assumed in the natal dispersal distances population classifications.

    5.        I would like to see some discussion on the natal dispersal assignment rate – why the French assignment rate was so low, and what might be causing the disparity between the two metapopulations.

    6.        There should be some acknowledgement that the individuals assigned as offspring may not be offspring – i.e. previously uncaptured colony members or colony visitors.

    7.        Mating dispersal in the manuscript is defined as the temporary movements of an individual from their resident roosts to mate, yet is quantified as the distance between father and offspring roosts, which inherently includes the distance travelled by the mother in mating. The discussion also focuses on the male movement. We cannot assume that the females are not also moving long distances; this should be addressed in the discussion.

    8.        The manuscript includes males that have fathered multiple young. It would be interesting to compare the maternity of the pups, to explore the potential of mating bonds.

    Minor comments

    1.        It would be useful to have a map of the sampling sites.

    2.        I would like to see some discussion of the bias of sampling only at maternity colonies, as you would assume this would have a large effect on paternity capture. This could include a discussion on the difficulties on sampling additional males, e.g. bachelor colonies, if that was a drawback.

     

    This review was compiled with the help of comments from my lab group.

  4. Peer Community in Evolutionary Biology

    The study of dispersal is crucial for understanding population dynamics, gene flow, and evolutionary trajectories in organisms. Dispersal mechanisms vary widely among species, leading to a complex interplay of genetic exchange and population structure. In this context, the article titled "The geometry of gametic dispersal in a flying mammal, Rhinolophus hipposideros" is a significant contribution to our understanding of dispersal dynamics in natural populations.

    Dispersal is not just the movement of individuals but involves the movement of genetic material. This study focuses on the lesser horseshoe bat, a species characterized by limited dispersal capabilities, male-biased dispersal, and genetic structure at fine spatial scales. The significance of this work lies in its exploration of two critical types of dispersal—natal and mating—and their combined effects on gene flow.

    I was particularly interested in how the authors disentangle the contributions of natal and mating dispersal to the overall gene flow in this study. They utilized advanced molecular techniques to investigate genetic structures, with the aim to assess how these two forms of dispersal interact to shape population dynamics—a topic rarely assessed.

    The methodologies included maternity and paternity analysis and genetic assignment techniques, to assess both natal and mating dispersal separately. This approach allowed them to construct a comprehensive model of dispersal distance kernel for the species, seperately for male natal and male mating dispersal. They used molecular data from colonies across two distinct metapopulationsto draw broader conclusions about dispersal behavior and genetic structure.

    The study revealed that approximately 50% of mating events in lesser horseshoe bats involved males traveling significant distances from their natal colonies, suggesting that mating dispersal plays a critical role in gene flow. The results showed a mean mating dispersal distance of about 11 km and a mean gametic dispersal distance of 20 km. The fat-tailed distribution of dispersal distances indicates that long-distance dispersal events, while rare, can have substantial impacts on gene flow and genetic structure. This highlights how even infrequent, long-distance dispersal can influence genetic diversity and connectivity among populations, underscoring the complexity of population dynamics.

    After positive reviewer comments I decided to accept the role of recommender for this article because it provides increased understanding of dispersal that integrates both natal and mating strategies. The methodology employed in this study, the application of genetic data, contributes to our understanding of dispersal dynamics in the field. Moreover, the results on the rare long-distance dispersal events highlights how such occurrences might influence genetic variation and population stability. 

    In conclusion, this study provides valuable insights and its findings may inform future research efforts exploring the dynamics of population genetics in various species.

    References

    Thomas Brazier, Diane Zarzoso-Lacoste, Lisa Lehnen, Pierre-Loup Jan, Sebastien J. Puechmaille, Eric J. Petit (2026) The geometry of gametic dispersal in a flying mammal, Rhinolophus hipposideros. bioRxiv, ver.2 peer-reviewed and recommended by PCI Evolutionary Biology https://doi.org/10.1101/2024.10.24.620000

  5. Version published to 10.1101/2024.10.24.620000 on bioRxiv