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  1. Evaluation Summary:

    This paper is of interest to organismal biologists and evolutionary scientists who study cognitive and behavioral sex differences including those with interests in the evolution of complex spatial behaviors. Using intensive field monitoring and experimentally induced navigational challenges, the authors examine two different hypotheses for sex differences in spatial ability in three species of poison frog. A rich and complex story emerges, including from the provision of evidence that is consistent with (but not necessarily yet definitively or exclusively in support of) the hypothesis that androgens may inadvertently affect spatial ability.

    (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 #2 agreed to share their name with the authors.)

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  2. Reviewer #1 (Public Review):

    Pašukonis et al. sought to differentiate the explanatory power of two major hypotheses for sex differences in navigational ability: the adaptive specialization hypothesis, which links home range size and navigational ability, and the androgen spillover hypothesis, which links testosterone in males to navigational ability. To examine these alternative hypotheses, the authors quantify home range size, testosterone levels, and successful homing following translocation using three species of poison frog. Of particular interest, the authors were able to contrast species that vary in which sex has the larger home range, potentially disambiguating the relationship with androgens versus home range size, a feature that is lacking in many prior studies of sex differences in spatial ability. [While the authors cite one notable exception (Guigueno et al., 2014 on spatial ability in female cowbirds), they did not give this prior study as much weight as they probably should have.]

    In many ways, this present study is a tour-de-force of field biology. Particular strengths include:

    1. The combination of field-based observations with experimental intervention. Using intensive monitoring of individuals in the rainforest, the experimenters were able to delineate the size of home ranges, the maximum extent of movement, as well as specific behaviors (e.g., mating, parental transport of tadpoles) associated with different movement distances. This is particularly astonishing when extended to three different species.

    2. The use of a natural navigational task. To assess navigational ability, the authors translocated individuals from their home ranges and determined the accuracy of, and success in, homing. While translocation is not exactly a natural experience (except for the rare occurrence, e.g., during an unusual flood), homing certainly is. Therefore, the author's assay tests wild animals in a real-world navigation problem. While the need for studying "cognition in nature" is widely recognized, it is often difficult to achieve.

    3. The inclusion of multiple species that, while closely related, vary in sex roles. The authors include two species in which the male is predicted to have larger home ranges and one in which the female is predicted to do so. The potential strength of this feature is that it allows the authors to contrast the explanatory power of the adaptive specialization hypothesis - which would predict the sex with the larger home range will be more accurate and successful in homing - with the androgen spillover hypothesis - which would predict males (with their higher androgen levels) to be more accurate and successful in homing, regardless of home range size.

    While the study offers a thorough and complex view of space-use and navigation in poison frogs, the study is held back by some weaknesses:

    1. The comparison of accurate/successful homing across species is hampered by the application of discrete displacement distances that are not scaled to the species' natural movements. The three study species, chosen for their differences in reproductive sex roles, also differ considerably in their natural range of movements. Exploratory movements, whether near or far, give individuals the necessary experiences that familiarize them with areas so that later they can successfully/accurately return home from those areas. As a consequence, displacing O. sylvatica by 50 meters - a distance that may well be outside the range of prior experience - is unlikely to have the same significance as displacing A. femoralis by 50 meters - a species that regularly move tens of meters in a day. Species differences in accuracy/success in homing may simply reflect differences in experience, but not differences in spatial ability.

    2. The authors' main conclusion is that their results contradict the adaptive specialization hypothesis for sex differences, but their results are more complex. Oophaga sylvatica is the one study species that provides the best test of this hypothesis, as the females have larger home range sizes and lower androgens. Yet, their results with O. sylvatica, in which males and females perform similarly in homing (i.e., there is a high p-value for the effect of sex), invite us to suspend judgement as to whether the sexes differ, rather than contradicting the adaptive specialization hypothesis. Not supporting one hypothesis does not necessarily lend strong support to the alternative hypothesis. Combined with the potential methodological shortcoming of using displacement distances that are not scaled to movement distances in O. sylvatica, caution is warranted.

    The relationship between androgens and exploratory behaviors is an important addition to our understanding of the complexity of sex differences in spatial ability and these results do indeed provide indirect support for the androgen spillover hypothesis. Yet, more work needs to be done to disambiguate these two hypotheses in this group. Further, the authors may want to consider that both hypotheses are simultaneously at play, contributing to different features of navigation in the two sexes, and/or that the different species won't necessarily follow the same rules.

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  3. Reviewer #2 (Public Review):

    Pašukonis et al. investigated the role of sex differences in androgen levels and parental care styles on sex differences in way-finding ability in three species of poison frogs. This was a direct test of the dominant hypothesis that the sex within a species with greater ecological demands to navigate effectively over greater distances (typically, males for reasons of mate-seeking, dispersal, or subsistence) against an alternative hypothesis that androgens may affect spatial ability regardless of any selection pressures. Hormones are well known to have non-adaptive side effects. Three frog species were chosen based on their generally similar ecology that critically differed with respect to the sex of which parent entailed obligate transportation or mobility (A. femoralis, predominantly male; D. tinctorius, entirely male; O. sylvatica, entirely female). Consistent with spillover, androgen levels predicted homing accuracy but parenting sex did not. This is the first experimental evaluation of androgen spillover in a species comparison.

    As a complex behavior, navigational ability is multiply-determined. Therefore, no single experiment can definitely identify and establish the causes at work. However, Pašukonis et al. have produced clear evidence that androgens play a role in shaping some sex differences regardless of the purported ecological drivers.

    Strengths
    1. Translocation is an excellent choice for measuring spatial ability because it is a highly naturalistic measure. The external validity is likely high.
    2. The species were well chosen. With the exception of predator threat, the three species are highly similar and therefore differences between them are less likely to be attributed to ecological or phylogenetic variation.
    3. The figures relating to home range, space use, and navigation are clear and easy to read. They may pose a challenge to those who view a black and white printed or displayed version and possibly those with color blindness, however.

    Weaknesses
    1. Multiple ways to measure home range are quite welcome, but more discussion or investigation about why these measures differ substantially when they do and what import this could have for past and future studies would improve the paper.
    2. The characterization of the current literature on human and some animal sex differences in spatial ability could be more complete. For example, cross-cultural studies on human populations (most of them fairly recent) suggest that individual factors of ranging due to subsistence mode and culture are powerful explanatory inputs that can erase sex differences entirely. The adaptive specialization hypothesis has failed to explain observations on Ovalentaria fishes such as cichlids and blennies.
    3. The species were well chosen for this analysis. However, as relatively close evolutionary relations, it becomes possible that observed patterns of traits do not generalize outside of their clade. This is not a criticism per se, but a caution about interpretation.

    Adaptation hypotheses can be so intuitive as to be beguiling. This is not an indicator of quality, but it should be an inducement to greater caution and skeptical rigor. The adaptive specialization hypothesis was arguably accepted by the late 80s. It was held by consensus as the explanation for human sex differences in spatial cognition based almost entirely on western samples. It was accepted as the explanation for a similar pattern in other animals based on a large majority of studies of laboratory animals and other rodents. Few alternative explanations had been proposed, let alone evaluated empirically, particularly non-adaptive explanations. While high-quality and dissenting papers have appeared in the last 15 years, the history represents a failure to apply an appropriately objective attitude toward investigation by accepting conclusions based on inadequate evidence, and a failure to pursue methods necessary for proper hypothesis testing such as cross-cultural and cross-species comparisons.

    The importance of the current study is not merely the investigation of an alternative hypothesis, but a testament to the importance of this critical element of inquiry in advancing knowledge. We may easily imagine that had the authors examined only Allobates femoralis, the data would have been taken as firm evidence for the adaptive specialization hypothesis. We are also left to wonder how often other researchers found unexpected results such as Oophaga sylvatica and consigned it to the file drawer or to published obscurity. The superior design that is a proper test rather than merely a confirmation of expectations has profited a richer view. Whether androgen spillover prevails as an explanation or not, the current work strongly suggests that the dominant model is at the very least incomplete. Further testing of this and other explanations are warranted for the adaptive specialization hypothesis as well as numerous other highly intuitive, largely accepted, but inadequately tested hypotheses. The opportunity before us is to help enhance the rigor and integrity of evolutionary inquiry sciences as a whole.

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