Male chickadees with better spatial cognition sire more extra-pair young

  1. Carrie L Branch
  2. Benjamin R Sonnenberg
  3. Joseph F Welklin
  4. Bronwyn G Butcher
  5. Virginia K Heinen
  6. Angela M Pitera
  7. Lauren M Benedict
  8. Eli S Bridge
  9. Irby J Lovette
  10. Michael S Webster
  11. Vladimir V Pravosudov

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    eLife Assessment

    This fundamental study examines the benefits of spatial cognition in a wild population of mountain chickadees. Using robust genetic analyses and experimental design, the authors show with compelling evidence that females seeking out extra-pair copulations prefer males with strong spatial cognition, and that these males have a reproductive advantage over other males. This work will be of broad interest to evolutionary and behavioural biologists.

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Abstract

Across animal taxa, females commonly mate with more than one male, even in monogamous mating systems. These extra-pair copulations and resulting young may increase the fitness of the female via a variety of mechanisms. The ‘good genes’ hypothesis suggests that socially monogamous females mate outside their pair bond to increase the fitness of their offspring via indirect genetic benefits, because extra-pair males do not provide parental care. We tested this hypothesis by quantifying extra-pair paternity in nonmigratory, food-caching mountain chickadees (Poecile gambeli). Chickadees rely on spatial cognition to recover scattered food caches and variation in spatial cognition is associated with increased survival, longer lifespan, and is heritable. However, less is known about the role of sexual selection on spatial cognitive abilities. In the current study, we found that 1. males with better spatial cognitive abilities sired more extra-pair young and produce heavier offspring in their own nests compared to their poorer performing counterparts, and 2. extra-pair males had significantly better spatial cognition than the social males they cuckolded. These results suggest that sexual selection shapes the evolution of spatial cognition in food-caching chickadees and are consistent with the good genes hypothesis, which posits that females gain indirect genetic benefits via extra-pair young.

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  1. Version published to 10.7554/elife.110905.2 on eLife
  2. Version published to 10.7554/elife.110905 on eLife
  3. eLife

    eLife Assessment

    This fundamental study examines the benefits of spatial cognition in a wild population of mountain chickadees. Using robust genetic analyses and experimental design, the authors show with compelling evidence that females seeking out extra-pair copulations prefer males with strong spatial cognition, and that these males have a reproductive advantage over other males. This work will be of broad interest to evolutionary and behavioural biologists.

  4. eLife

    Reviewer #1 (Public review):

    This study demonstrates sexual selection on spatial cognition via extra-pair paternity in socially monogamous, non-migratory mountain chickadees (Poecile gambeli). Males rely on spatial memory to recover food caches, with abilities linked to survival, longevity, and heritability. In a wild population, authors quantified extra-pair young (EPY) and compared the cognition of extra-pair sires to cuckolded social males using feeder-array assays. Better-performing males sired more EPY and heavier offspring in their nests; extra-pair sires significantly outperformed social males. Results support the good-genes hypothesis: females gain indirect genetic benefits via EPY from cognitively superior mates.

  5. eLife

    Reviewer #2 (Public review):

    Summary:

    In this study, the authors ask whether spatial cognition is under sexual selection in mountain chickadees. To do so, the authors examined a large dataset that includes a) spatial cognition data for both males and females (obtained via use of a clever RFID-based feeder system) and b) social and extra-pair paternity nesting data. As predicted, males with higher spatial cognition sired more extra-pair offspring, and extra-pair sires had, on average, higher spatial cognition scores than the males they cuckolded. Interestingly, females with lower spatial cognition scores were more likely to seek extra-pair copulations, potentially to compensate for their own low spatial cognition. Surprisingly, there was no difference in spatial cognition scores between males that sired their own offspring and those that lost paternity at the nest. Also surprising was the fact that there were no differences in patterns of extra-pair paternity and spatial cognition between high- and low-elevation sites. The latter is particularly surprising in that spatial cognition should be under stronger selection at the high elevation site. Overall, this is a fascinating study that demonstrates that spatial cognition - a trait under natural selection as it directly impacts winter foraging and survival behaviour -is also under sexual selection.

    Strengths:

    The authors have a robust dataset (n = 732 offspring sampled over 3 years), high-quality spatial cognition data collected with a procedure that has been well-honed over the years, and couple the data with solid statistical procedures that address many potential covariates and potentially confounding factors. In addition, the authors are careful in the discussion to elaborate on the many potential alternative explanations from the results and questions that are likely to arise in the minds of readers (e.g., how are females assessing male spatial ability?)

  6. eLife

    Reviewer #3 (Public review):

    Summary:

    The authors presented evidence that spatial cognition in this population is under sexual selection, with extra-pair males, primarily chosen by the females, having better spatial cognition than males they cuckolded and males with better spatial cognition having more extra-pair young.

    Strengths:

    This cognitive ecology study was conducted on a well-known long-term study population of free-ranging mountain chickadees. This strong base, alongside a thorough study design and extensive statistical analyses, enabled the authors to address research questions that few other labs can address, making this a potentially powerful study of broad general interest.

  7. eLife

    Author response:

    The following is the authors’ response to the original reviews.

    Public Reviews:

    Reviewer #1 (Public review):

    This manuscript presents compelling evidence from a wild chickadee population linking heritable spatial cognition to extra-pair paternity success, supporting sexual selection via good genes in a food-caching species. The integration of RFID cognition tests with ddRAD paternity assignment is methodologically strong and timely for behavioral ecology, though causal mechanisms and confounds warrant clarification.

    Overall, a major revision of the manuscript is recommended, addressing the points below.

    (1) Confirmation of manipulation and treatment effects.

    The central claim hinges on spatial cognition driving EP siring, but direct evidence that cognition predicts observed copulations (vs. post-copulatory mechanisms) is absent. While territories do not cluster by performance (Figure S4), quantify male aggression/movement data during fertile periods to rule out intrusion-based EPP. The authors should provide metrics like nearestneighbor distances for EP sires or playback responses linking cognition to dominance, as in prior chickadee work. Without this, causal female preference remains correlational.

    We do provide the mean distance to all known EP sires in Figure S2, in addition to the known neighbors coded by cognition and EPP (Figures S3 and S4). Unfortunately, we do not have data with playbacks for this set of individuals, though we have shown that males respond to threats from high or low elevation birds equally, which provides a potential proxy for cognitive performance and dominance (e.g., high elevation birds perform better on the task than low elevation birds, and low elevation birds are dominant/,more aggressive than high elevation birds; Kozlovsky et al. 2014, Beh Ecol and Sociobiol; Branch et al. 2015, Behaviour; Branch & Pravosudov 2016, Ethology).

    As mentioned in discussion of the manuscript, we do not see a significant relationship between dominance and task performance in our system (Heinen et al 2021) – this is also true for the closely-related black-capped chickadees (Robayo Noguera et al 2025). This is not to say that social dominance status does not affect female preference or choice, but that data is outside the scope of this work. We would like to highlight that we’ve shown high repeatability in individual task performance and shown a strong gene c basis for spa al learning and memory performance (Sonnenberg et al. 2019; Branch et al 2022; Semenov 2024, Current Biology). While social dominance status is a rela ve trait and known to change with me and age (eg adults are dominant to juveniles).

    From discussion:

    “Furthermore, while higher social dominance status is associated with access to better territories in chickadees (86), we see no association with dominance status and spatial cognitive abilities in our system (46) or closely related black-capped chickadees (81). While it is possible that our results reflect some unmeasured trait(s) linked to spatial cognitive ability, such as boldness, aggression, or increased exploratory behavior (e.g., 32), previous data from our system do not support these additional alternative hypotheses. Chickadees with enhanced spatial cognitive abilities are not more aggressive (78) nor do they show higher rates of exploratory behavior (e.g., higher space use) (79).”

    We agree that the results we present are correlational. A causal relationship is outside the scope of this research, as we cannot manipulate cognition in the wild and chickadees will not breed in captivity. The strength of our approach lies in multi-year data collection and the ability to compare among the social and extra-pair males, as well as using what we know about the system and species to rule out additional explanations, including age.

    (2) Female cognition-EPY link inconsistency.

    Poor female cognition predicts more EPY (first-20-trials: offspring-level χ2=6.21, P=0.013; nests: χ2=6.79, P=0.009), but not for full-task (P>0.5). The authors should discuss why (e.g., learning speed vs. memory stability) and add exploratory correlations (female errors vs. EPY proportion). They should soften claims in the Discussion section of "female-driven" without consistent support and should frame this as a hypothesis.

    Absolutely, we agree that this is an interesting nuance to the results regarding female cognition. While number of errors on the first 20 trials and across the entire task are highly correlated, this is not a 1-to-1 relationship (Figure S7a). We suggest that performance in the first 20 trials reflects memory acquisition, while performance across the full task reflects memory retention and recall (Sonnenberg et al. 2019) – both critical components of spatial learning and memory for food-caching birds.

    Previous work has shown that performance in the first 20 trials and across the entire task is linked to survival (Sonnenberg et al. 2010) and longer lifespan (Welklin et al. 2024) – meaning both metrics reflect fitness. In the discussion, we suggest females may be compensating for their poorer abilities by seeking EPY, but this is speculative, as we do not have data beyond the correlative relationship we report and cannot provide more insight to the difference between the first-20 and entire task. This said, it is not only poor performing females that have EPY in the nest and we included the female/mother identity as a random factor in our models (see Statistical analysis section of Methods). Certainly, further investigation into female task performance and mate choice is warranted.

    Edit to MS:

    In the discussion we have edited the sentence to be more specific to our findings:

    “Indeed, females with poorer spatial memory acquisition (made more errors on the first 20 trials) had more extra-pair young in their nests, while social male cognitive performance did not predict EPY in the nest.”

    (3) Cognitive task sensitivity and validity.

    Mean errors aggregate learning curves effectively, but single feeder-assignment (nonpreferred) confounds neophobia/motivation with spatial ability. The authors should report trial-by-trial improvements (Figure S7 subset) or criterion-to-learn metrics. Justify excluding high-error birds (<3 mean); sensitivity analysis needed to check bias toward high performers.

    We respectfully disagree that our task lacks sensitivity or validity. The criterion-to-learn or trials-to-criterion metric has been criticized for decades and should not be used in studies comparing individual variation, in our opinion (e.g., Pravosudov 2022, Current Opinion in Behavioral Science; Harrington & Lambert 2025, Biology Letters).

    We use metrics based on the nature of our task to assess performance and ensure birds have learned before we include them in our analyses, for instance, all birds made < 3 errors on average and completed at least 20 trials. Random chance performance on our task is 3.5 errors (7 possible errors), therefore, birds that make more than 3 errors have not learned the task and therefore would not be included in analyses. It should be noted that this is very rare and typically if birds are excluded its because they do not complete 20 trials.

    See Testing spatial cognition section of the manuscript:

    “In addition, birds were included in analyses if they performed at least 20 trials and made fewer than mean 3 errors across the 4-day testing period.”

    We can certainly understand concerns about individual differences in motivation and neophobia, however, we have also considered this and made efforts to address these issues. That said, we do rely on birds to participate willingly in the spatial task and there may be some bias associated with those that participate vs. those that do not that we cannot account for. Chickadees, as a caching species, are particularly well-suited for our work as they appear to have infinite motivation to obtain and store food items in the wild (and individuals indeed differ in this, hence the differences in the number of trials completed, which we control for in our analyses). We know this not only from our study but work from many researchers, where birds have ad libitum food and continue to cache. Regarding neophobia, birds are introduced to the feeder array in stages, as we explain in the methods, and no humans are present during testing.

    “Each array consisted of eight equidistant RFID-based feeders on a square (122 x 122 cm) aluminum frame suspended ca. 4 m above the ground (Figure 1). Each feeder is equipped with a small, motorized door. Prior to testing, we kept the feeder doors of the arrays open for approximately one month. Next, the feeder doors were closed and programmed to open for any bird with a PIT tag, this allowed birds to habituate to the motorized feeder doors for one week. Finally, we measured the spatial learning and memory abilities of mountain chickadees using a 4-day task. The spatial learning and memory task involved pseudo-randomly assigning each bird to a single feeder in the 8-feeder array that was not its most-visited feeder during the previous two habituation stages.”

    Finally, using the first-20 and 4-day task performance metrics we’ve shown relationships between survival, longevity, genetic variation, and reproductive output, while seeing none of these relationships with the cognitive flexibility task (all with different groups of birds over the years), which we find to be the most compelling evidence that our metric is valid and sensitive.

    (4) Paternity assignment robustness.

    ddRAD-CERVUS with bimodal LODs (Figure S8) is solid, but unassigned EPY (social-genotyped but no sire) implies missing sires (~?% of EPY?). Include all alive males as candidates yearly? Test power simulations for LOD thresholds. 2019 exclusion justified, but multi-year SNP alignment could boost resolution.

    One of the limitations or challenges of our system is that the birds inhabit a highly contiguous forest and our field site is not demarked by boundaries or barriers, meaning we do have undetected males just outside our field site that likely sire offspring and we have no data for. That said, we were able to assign paternity to 630 out of 732 offspring, giving us a success rate of 86%. We have now added this to the first paragraph of the results. For all 732 chicks we knew the social males genotype and could ID presence of EPY, but in that 14% we could not ID the EP male specifically. We did include all alive males as potential sires. This includes males that may not have been nesting in our boxes that particular year, but were detected alive in the previous winter testing season that we were able to genotype.

    We tried a multi-year SNP alignment first, but obtained stronger paternity assignments and differentiation between first and second-tier candidate sires when we ran each year separately. Running the SNP analysis for each year separately resulted in more SNPs to use in each year which increased our ability to confidently assign paternity.

    (5) Mechanistic speculation vs. data.

    Discussion invokes hippocampus genes (GWAS priors) and good genes, but no offspring cognition/survival data. Label as hypotheses; suggest tracking EPY recruitment. No brood size costs for EP sires is key, but monitor long-term nest investment (e.g., feeding rates).

    Indeed, these are informed speculations/hypotheses based on our previous work showing the genetic bases of cognition and high levels of heritability (Branch et al 2022; Semenov 2024, Current Biology). We also know that juvenile survival is predicted by performance on our spatial cognitive task (Sonnenberg et al 2019, Current Biology). However, we do not have offspring survival for these particular EPY (past fledging the nest). We recruit about 5% of the young back into our study site (Whitenack et al. 2025), which makes it difficult to make meaningful inferences at this point. Though, as we continue to collect data in this system we hope to obtain a sample size to address these questions.

    We have collected data on feeding rates at the nest via RFID in some years, however, these measures come with additional caveats as they do not control for the amount/quality of food. Though, preliminary analyses suggest no difference in feeding rates based on cognitive abilities.

    We use the mass of the nestlings at Day 16, which is a common proxy for survival likelihood in Passerines, and we know individuals of higher mass are more likely to survive and be recruited back into the system (Whitenack et al. 2025).

    Reviewer #2 (Public review):

    Summary:

    In this study, the authors ask whether spatial cognition is under sexual selection in mountain chickadees. To do so, the authors examined a large dataset that includes a) spatial cognition data for both males and females (obtained via use of a clever RFID-based feeder system) and b) social and extra-pair paternity nesting data. As predicted, males with higher spatial cognition sired more extra-pair offspring, and extra-pair sires had, on average, higher spatial cognition scores than the males they cuckolded. Interestingly, females with lower spatial cognition scores were more likely to seek extra-pair copulations, potentially to compensate for their own low spatial cognition. Surprisingly, there was no difference in spatial cognition scores between males that sired their own offspring and those that lost paternity at the nest. Also surprising was the fact that there were no differences in patterns of extra-pair paternity and spatial cognition between high- and low-elevation sites. The latter is particularly surprising in that spatial cognition should be under stronger selection at the high elevation site. Overall, this is a fascinating study that demonstrates that spatial cognition - a trait under natural selection as it directly impacts winter foraging and survival behaviour -is also under sexual selection.

    Strengths:

    The authors have a robust dataset (n = 732 offspring sampled over 3 years), high-quality spatial cognition data collected with a procedure that has been well-honed over the years, and couple the data with solid statistical procedures that address many potential covariates and potentially confounding factors. In addition, the authors are careful in the discussion to elaborate on the many potential alternative explanations from the results and questions that are likely to arise in the minds of readers (e.g., how are females assessing male spatial ability?)

    Weaknesses:

    Overall, no major weaknesses were identified in this study. As always, there are editorial issues that I would encourage the authors to consider, including presentation of data/results and clarification on some statistical issues. Overall, however, this is an excellent study that will make an important contribution to our understanding of the evolution of cognition and targets of sexual selection.

    Reviewer #3 (Public review):

    Summary:

    The authors presented evidence that spatial cognition in this population is under sexual selection, with extra-pair males, primarily chosen by the females, having better spatial cognition than males they cuckolded and males with better spatial cognition having more extrapair young.

    Strengths:

    This cognitive ecology study was conducted on a well-known long-term study population of free-ranging mountain chickadees. This strong base, alongside a thorough study design and extensive statistical analyses, enabled the authors to address research questions that few other labs can address, making this a potentially powerful study of broad general interest.

    Weaknesses:

    Throughout the manuscript, there is a focus on the "mean number of location errors per trial over the first 20 trials". Performance changes across trials, so why weren't learning vs peak performance analyzed separately? Similarly, authors also describe results in the context of the entire task, but sometimes in the context of the first 20 trials - why is one prioritised over the other, and why is the emphasis not always consistent? Are the results across the two generally the same? A more thorough explanation addressing all these points is necessary.

    Results are often similar in both metrics, however, the relationship between first 20 and total trials is not 1 to 1 (reported at top of results section and Figure S7a). We suggest that performance in the first 20 trials reflects memory acquisition, while performance across the full task reflects memory retention and recall (Sonnenberg et al. 2019) – both critical components of spatial learning and memory for food-caching birds. Previous work has shown that performance in the first 20 trials and across the entire task is linked to survival (Sonnenberg et al. 2010) and longer lifespan (Welklin et al. 2024) – meaning both metrics reflect fitness.

    We did locate several instances where the metric used is not clear and we have corrected this, thank you.

    To summarize, we reported results for both metrics for analyses related to the main hypotheses, and then reported first-20 trials in the main text for additional tests and provided the entire test data in the Supplemental Materials.

    Lines 429-432: Why was a categorical (i.e., chi-square test) and not a numerical comparison implemented? A numerical statistical test would capture more of the variation (i.e., the number of years separating the social and EPY males).

    We agree and have added a paired t-test to assess whether within each offspring, the social father differed in age from the EP father. This test returned a similar result (χ21=0.27, P=0.662) and has been added to the results.

    Recommendations for the authors:

    Reviewer #2 (Recommendations for the authors):

    (1) Statistical analysis:

    The authors include elevation as a fixed effect in their models; however, I am curious as to why there were no elevation interaction terms included in the model, as I would predict that selection for higher spatial cognition would be stronger in high-elevation sites.

    We did test for an interaction between elevation and cognition in many of our models and did not find any support for interactions. For example, there was no interaction between elevation and cognition in the number of EPY sired model.

    (2) General comments:

    (a) I would prefer to see extra-pair paternity written out rather than EP, EPY, EPP, etc., as the inclusion of the words takes little extra space in the text and makes for easier reading (personal preference).

    We agree and have spelled out EP, EPY, EPC, and EPP throughout the MS.

    (b) The discussion does an excellent job addressing these questions, but it could be worth noting in the introduction why it is unlikely that this pattern would result simply from selection for dominance (or other factors), given that readers familiar with chickadees would likely immediately think about the role of dominance in extra-pair paternity.

    We have added this point to the introduction, thank you:

    “Previous research in chickadees shows that females often produce extra-pair young with socially dominant males (e.g., 44, 45), however, in our study system we do not see a significant relationship between social dominance and spatial cognitive abilities (46). One potential explanation for this, is that social dominance changes over an individual’s lifetime and with age, while spatial cognition is repeatable and consistent over individual mountain chickadee’s lifetime (25, 27-32).”

    (3) Specific comments:

    (a) Line 27-31: This feels like a weak justification. The study is really about selection on cognition rather than the study of sexual selection per se. I would encourage the authors to revise this justification statement to focus on how sexual selection can help shape cognition.

    We have edited the abstract.

    (b) Line 49: Suggest a stronger start rather than justifying the paper by stating that mate choice has been a focus of evolutionary biology.

    We have edited this statement.

    (c) Line 50: I believe this should be "mate choice" rather than "sexual selection"

    Edited.

    (d) Line 59-62: Confusing wording throughout, especially as "high quality" does not refer to sperm competition, but rather sperm that may have an advantage during sperm competition.

    Suggest reworking the sentence for clarity.

    We changed this to quality instead of competition.

    (e) Line 69: Predictable variation in what?

    We have removed predictable variation.

    (f) Line 87: time;

    Corrected.

    (g) Line 104: Cut "specifically (i.e., caches are not used for provisioning young),".

    Removed.

    (h) Line 106: Presumably referring to assortative mating?

    Added.

    (i) End of the introduction focuses on a couple of primary questions; however, once the reader gets to the methods and results, we find many more tests (e.g., age, brood size, female cognition, etc.). If the authors are going to include these additional tests (which I think they should), then I encourage them to provide the predictions or justifications for those analyses here. In addition, please double-check to ensure the presentation of all tests is consistent throughout the intro/methods/results/discussion.

    We have now added this information to the end of the introduction as alternative explanations, rather than specific predictions. These additional analyses were implemented post-hoc to exclude alternative explanations for the patterns observed, but we have linked them to the statistical analyses as requested by Reviewer 3 and for clarity.

    (j) Suggest including sample size (nests, nestlings, etc. per year) in methods.

    We have provided all sample sizes in the Supplemental Tables and in the text where appropriate.

    (k) Line 255: How many egg dumps? Would be interesting to have a number here for future meta-analyses, reviews, BOTW accounts, etc.

    Unfortunately, we do not have this data available, and the numbers were very low which is why we did not report them in the manuscript. As we continue to work in the system we will be able to provide this information.

    (l) Line 273: See comment above re: elevation as an interaction term in models.

    Addressed above.

    We did test for an interaction between elevation and cognition in many of our models and did not find any support for interactions. For example, there was no interaction between elevation and cognition in the number of EPY sired model.

    (m) Line 282: extra period.

    Removed.

    (n) Line 328: Change "Here" to "Next".

    Edited.

    (o) Line 465: I would suggest bringing this in earlier and considering the flow of how ideas are presented. Seems more logical to first look at whether males lost paternity, then, if so, to whom those males lost paternity.

    We have reorganized the results section to be consistent with the stats methods order.

    (p) Line 553: suggest "likely means" as there may be other attributes of individual quality outside of spatial cognition that are important.

    Yes, we have added this qualifier.

    Reviewer #3 (Recommendations for the authors):

    (1) Section starting at line 268: This section has a long list of statistical analyses. To better help the reader follow the aims of the study and the relationship between them, I recommend numbering the research questions in the introduction and pairing them with the description of each statistical test here in the Statistical Analyses section.

    We agree, thank you for this suggestion.

    We have now added this information to the end of the introduction as alternative explanations, rather than specific predictions. These additional analyses were implemented post-hoc to exclude alternative explanations for the patterns observed, but we have linked them to the statistical analyses and results as requested.

    (2) Lines 295-297: What was the percentage of tested individuals that had brood size data available?

    We only have brood size information for birds that breed in our nestboxes and make it to day 16 post-hatching – this is a much-reduced sample from those that participate in cognitive testing (we test around 150 birds a year between both elevation sites). In addition, throughout breeding stages we lose nests to predation, prior to day 16, when we collect blood samples from the chicks. Birds also participate in cognitive testing and breeding in multiple years, so our sample size for EPP is a result of repeated measures in some instances.

    (3) Lines 473-479: The study is done, so use the past tense throughout the manuscript.

    Thank you, we have edited this for consistency.

  8. Version published to 10.1101/2025.09.30.679593v3 on bioRxiv
  9. Mentioned by @lucresnooker.bsky.social on Bluesky

    the shape rotators have gone too far this time elifesciences.org/reviewed-pre...

  10. Mentioned by @cognitiveecol.bsky.social on Bluesky

    New paper - we show that in chickadees, males with better spatial cognition sire more extra-pair young and that when a female has an EPY, it is sired by a male with better spatial cognition compared to cognition of her social mate. elifesciences.org/reviewed-pre...

  11. Version published to 10.7554/elife.110905.1 on eLife
  12. eLife

    eLife Assessment

    This important study examines the benefits of spatial cognition in a wild population of mountain chickadees. Using robust genetic analyses and experimental design, the authors show with compelling evidence that females seeking out extra-pair copulations prefer males with strong spatial cognition, and that these males have a reproductive advantage over other males. This work is of broad interest to evolutionary and behavioural biologists.

  13. eLife

    Reviewer #1 (Public review):

    This manuscript presents compelling evidence from a wild chickadee population linking heritable spatial cognition to extra-pair paternity success, supporting sexual selection via good genes in a food-caching species. The integration of RFID cognition tests with ddRAD paternity assignment is methodologically strong and timely for behavioral ecology, though causal mechanisms and confounds warrant clarification.

    Overall, a major revision of the manuscript is recommended, addressing the points below.

    (1) Confirmation of manipulation and treatment effects. The central claim hinges on spatial cognition driving EP siring, but direct evidence that cognition predicts observed copulations (vs. post-copulatory mechanisms) is absent. While territories do not cluster by performance (Figure S4), quantify male aggression/movement data during fertile periods to rule out intrusion-based EPP. The authors should provide metrics like nearest-neighbor distances for EP sires or playback responses linking cognition to dominance, as in prior chickadee work. Without this, causal female preference remains correlational.

    (2) Female cognition-EPY link inconsistency. Poor female cognition predicts more EPY (first-20-trials: offspring-level χ²=6.21, P=0.013; nests: χ²=6.79, P=0.009), but not for full-task (P>0.5). The authors should discuss why (e.g., learning speed vs. memory stability) and add exploratory correlations (female errors vs. EPY proportion). They should soften claims in the Discussion section of "female-driven" without consistent support and should frame this as a hypothesis.

    (3) Cognitive task sensitivity and validity. Mean errors aggregate learning curves effectively, but single feeder-assignment (non-preferred) confounds neophobia/motivation with spatial ability. The authors should report trial-by-trial improvements (Figure S7 subset) or criterion-to-learn metrics. Justify excluding high-error birds (<3 mean); sensitivity analysis needed to check bias toward high performers.

    (4) Paternity assignment robustness. ddRAD-CERVUS with bimodal LODs (Figure S8) is solid, but unassigned EPY (social-genotyped but no sire) implies missing sires (~?% of EPY?). Include all alive males as candidates yearly? Test power simulations for LOD thresholds. 2019 exclusion justified, but multi-year SNP alignment could boost resolution.

    (5) Mechanistic speculation vs. data. Discussion invokes hippocampus genes (GWAS priors) and good genes, but no offspring cognition/survival data. Label as hypotheses; suggest tracking EPY recruitment. No brood size costs for EP sires is key, but monitor long-term nest investment (e.g., feeding rates).

  14. eLife

    Reviewer #2 (Public review):

    Summary:

    In this study, the authors ask whether spatial cognition is under sexual selection in mountain chickadees. To do so, the authors examined a large dataset that includes a) spatial cognition data for both males and females (obtained via use of a clever RFID-based feeder system) and b) social and extra-pair paternity nesting data. As predicted, males with higher spatial cognition sired more extra-pair offspring, and extra-pair sires had, on average, higher spatial cognition scores than the males they cuckolded. Interestingly, females with lower spatial cognition scores were more likely to seek extra-pair copulations, potentially to compensate for their own low spatial cognition. Surprisingly, there was no difference in spatial cognition scores between males that sired their own offspring and those that lost paternity at the nest. Also surprising was the fact that there were no differences in patterns of extra-pair paternity and spatial cognition between high- and low-elevation sites. The latter is particularly surprising in that spatial cognition should be under stronger selection at the high elevation site. Overall, this is a fascinating study that demonstrates that spatial cognition - a trait under natural selection as it directly impacts winter foraging and survival behaviour -is also under sexual selection.

    Strengths:

    The authors have a robust dataset (n = 732 offspring sampled over 3 years), high-quality spatial cognition data collected with a procedure that has been well-honed over the years, and couple the data with solid statistical procedures that address many potential covariates and potentially confounding factors. In addition, the authors are careful in the discussion to elaborate on the many potential alternative explanations from the results and questions that are likely to arise in the minds of readers (e.g., how are females assessing male spatial ability?)

    Weaknesses:

    Overall, no major weaknesses were identified in this study. As always, there are editorial issues that I would encourage the authors to consider, including presentation of data/results and clarification on some statistical issues. Overall, however, this is an excellent study that will make an important contribution to our understanding of the evolution of cognition and targets of sexual selection.

  15. eLife

    Reviewer #3 (Public review):

    Summary:

    The authors presented evidence that spatial cognition in this population is under sexual selection, with extra-pair males, primarily chosen by the females, having better spatial cognition than males they cuckolded and males with better spatial cognition having more extra-pair young.

    Strengths:

    This cognitive ecology study was conducted on a well-known long-term study population of free-ranging mountain chickadees. This strong base, alongside a thorough study design and extensive statistical analyses, enabled the authors to address research questions that few other labs can address, making this a potentially powerful study of broad general interest.

    Weaknesses:

    Throughout the manuscript, there is a focus on the "mean number of location errors per trial over the first 20 trials". Performance changes across trials, so why weren't learning vs peak performance analyzed separately? Similarly, authors also describe results in the context of the entire task, but sometimes in the context of the first 20 trials - why is one prioritised over the other, and why is the emphasis not always consistent? Are the results across the two generally the same? A more thorough explanation addressing all these points is necessary.

    Lines 429-432: Why was a categorical (i.e., chi-square test) and not a numerical comparison implemented? A numerical statistical test would capture more of the variation (i.e., the number of years separating the social and EPY males).

  16. Version published to 10.1101/2025.09.30.679593v2 on bioRxiv
  17. Mentioned by @biorxiv-behav.bsky.social on Bluesky

    Seeking smarts: Male chickadees with better spatial cognition sire more extra-pair young https://www.biorxiv.org/content/10.1101/2025.09.30.679593v1

  18. Mentioned by @biorxivpreprint.bsky.social on Bluesky

    Seeking smarts: Male chickadees with better spatial cognition sire more extra-pair young https://www.biorxiv.org/content/10.1101/2025.09.30.679593v1

  19. Version published to 10.1101/2025.09.30.679593v1 on bioRxiv