Latest paper: social bet-hedging in vampire bats (and two other recent and related studies)

Our latest paper here.  Also some early press here. There are actually three recent papers on social networks and the benefits of network size in primates (by Laurent Brent and co-authors), songbirds (by Josh Firth and co-authors), and bats (by me and co-authors):

Family network size and survival across the lifespan of female macaques

by L. J. N. Brent, A. Ruiz-Lambides, M. L. Platt

Abstract: Two decades of research suggest social relationships have a common evolutionary basis in humans and other gregarious mammals. Critical to the support of this idea is growing evidence that mortality is influenced by social integration, but when these effects emerge and how long they last is mostly unknown. Here, we report in adult female macaques that the impact of number of close adult female relatives, a proxy for social integration, on survival is not experienced uniformly across the life course; prime-aged females with a greater number of relatives had better survival outcomes compared with prime-aged females with fewer relatives, whereas no such effect was found in older females. Group size and dominance rank did not influence this result. Older females were less frequent targets of aggression, suggesting enhanced experience navigating the social landscape may obviate the need for social relationships in old age. Only one study of humans has found age-based dependency in the association between social integration and survival. Using the largest dataset for any non-human animal to date, our study extends support for the idea that sociality promotes survival and suggests strategies employed across the life course change along with experience of the social world.

brent

From the world’s longest-running field study of birds at Oxford…

Wild birds respond to flockmate loss by increasing their social network associations to others

by Josh A. Firth, Bernhard Voelkl, Ross A. Crates, Lucy M. Aplin, Dora Biro, Darren P. Croft, Ben C. Sheldon

Abstract: Understanding the consequences of losing individuals from wild populations is a current and pressing issue, yet how such loss influences the social behaviour of the remaining animals is largely unexplored. Through combining the automated tracking of winter flocks of over 500 wild great tits (Parus major) with removal experiments, we assessed how individuals’ social network positions responded to the loss of their social associates. We found that the extent of flockmate loss that individuals experienced correlated positively with subsequent increases in the number of their social associations, the average strength of their bonds and their overall connectedness within the social network (defined as summed edge weights). Increased social connectivity was not driven by general disturbance or changes in foraging behaviour, but by modifications to fine-scale social network connections in response to losing their associates. Therefore, the reduction in social connectedness expected by individual loss may be mitigated by increases in social associations between remaining individuals. Given that these findings demonstrate rapid adjustment of social network associations in response to the loss of previous social ties, future research should examine the generality of the compensatory adjustment of social relations in ways that maintain the structure of social organization.

Given their relevance, if these papers had come out earlier, I would have cited them!

Social bet-hedging in vampire bats

by Gerald G. Carter, Damien R. Farine, Gerald S. Wilkinson

Abstract: Helping kin or nonkin can provide direct fitness benefits, but helping kin also benefits indirect fitness. Why then should organisms invest in cooperative partnerships with nonkin, if kin relationships are available and more beneficial? One explanation is that a kin-limited support network is too small and risky. Even if additional weaker partnerships reduce immediate net cooperative returns, individuals extending cooperation to nonkin can maintain a larger social network which reduces the potential costs associated with losing a primary cooperation partner. Just as financial or evolutionary bet-hedging strategies can reduce risk, investing in quantity of social relationships at the expense of relationship quality (‘social bet-hedging’) can reduce the risks posed by unpredictable social environments. Here, we provide evidence for social bet-hedging in food-sharing vampire bats. When we experimentally removed a key food-sharing partner, females that previously fed a greater number of unrelated females suffered a smaller reduction in food received. Females that invested in more nonkin bonds did not do better under normal conditions, but they coped better with partner loss. Hence, loss of a key partner revealed the importance of weaker nonkin bonds. Social bet-hedging can have important implications for social network structure by influencing how individuals form relationships.

(here’s all the text copied below)

1. Introduction

When cooperative relationships require an investment of time or energy, individuals should invest preferentially in the partner yielding the greatest cooperative returns [1–3]. However, if cooperative relationships take time to develop and partners are not always available, then a strategy that focuses investments in the single most-profitable partnership is risky. When partner availability is unpredictable, a better strategy would diversify cooperative investments across more partners to reduce the potential costs of losing a key partnership. We call this strategy social bet-hedging. Like other forms of bet-hedging [4], this strategy can be advantageous even if it reduces average short-term returns.

Bet-hedging strategies avoid risk. Social bet-hedging is analogous to evolutionary bet-hedging, where phenotypes with less temporally variable reproductive success outbreed phenotypes yielding reproductive success that is higher on average but more temporally variable [4]. This occurs because optimizing growth rates (or returns on investment) requires increasing the geometric, rather than arithmetic, mean. An evolutionary bet-hedging strategy can maximize geometric mean fitness, even at the expense of a lower arithmetic mean fitness, by coping better with rare stressful conditions [4].

By spreading cooperative investments to more partners, social bet-hedging strategies can reduce the temporal variance in cooperative returns caused by changes in partner availability. Investing in new relationships can be beneficial even if this requires diverting time and energy away from the most-profitable cooperative relationship which yields the greatest inclusive fitness return rate (e.g. the strongest reciprocator or closest kin).

Social bet-hedging might explain why female common vampire bats (Desmodus rotundus) that have strong reciprocal food-sharing relationships with close kin still regurgitate food to other nonkin [5–7]. Vampire bats are susceptible to starvation and depend on a network of food-sharing partners to feed them after unsuccessful foraging nights. The strongest, most reliable, and most balanced food-sharing bonds develop between mothers and daughters, but even for these close kin, the direct fitness benefits of food sharing might exceed the indirect fitness benefits [5–10]. The best known predictor of sharing rates within familiar pairs is not kinship, but the reciprocal rate of sharing [5,8]. If feeding close kin yields reciprocal sharing benefits that are equal or greater to feeding nonkin, why invest in nonkin bonds?

Sharing only with kin could be risky because relatives can be lost for various reasons. A starved female with only one or a few close maternal kin in her food-sharing network might not find her primary close kin donor, for example, if this partner also failed to feed or switched to a different roost on that night—which happens frequently [10]. To compensate for this risk, a social bet-hedging female would foster new bonds by diverting some of her social time and energy away from mothers and daughters and towards other females. Even if each of these additional partners is less related and reciprocates less, this strategy could dramatically increase long-term survival by reducing the risk of failing to find a primary donor when in dire need.

To test this idea, we quantify the impact, in terms of total food received, of removing a past key food donor for individual bats in need. Previously, Carter & Wilkinson [6] demonstrated that females that fed more nonkin females in previous years subsequently received more food in the absence of this key donor (see Methods), but this finding could simply mean that better-connected bats always receive more food. Here, we extend our analysis of this experiment to show that, as predicted by social bet-hedging, helping more nonkin did not increase food received when key donors were available, but it reduced the negative impact on food received when a key donor was removed.

2. Methods

We used data from a previous experiment [6], where a female subject was isolated and fasted for 24 h, then reintroduced to a captive colony of 27–34 individually marked conspecifics to measure food donated by each groupmate. Mean dyadic donation rates were calculated from 1337 dyadic regurgitation observations among 14 captive females using 91 fasting trials over a 4-year period (see electronic supplementary material, [6]). Relatedness was estimated using maternal pedigree and 19 microsatellite markers (see [6]). For each female, a unique key donor with a strong history of food sharing was selected for temporary removal; key donors were either the subject’s highest-ranking donor (nine cases), second-highest ranking donor (four cases), or a lower-ranking donor but the highest-ranking recipient (one case) (see electronic supplementary material, [6]). During two control trials, a female that had never fed the subject was excluded by either removing it or fasting it on the same night. During three subsequent test trials, the subject’s key donor was similarly excluded [6]. A previous analysis showed that bats that fed more nonkin females in past years received more food during test trials [6], but the social bet-hedging hypothesis predicts that this relationship should be most important when key donors are removed, not when they are present.

Here, we fitted linear models to predict the amount of food received with and without key donors present as well as the change in total food received (difference in food received per trial) when key donors were removed. We included the number of nonkin females fed in the past 4 years to represent investment in the size of a social support network. We did not include the number of kin fed because this depended on the number of kin available. We also did not include the number of males fed because stable bonds in the wild are female–female. To control for sampling bias, we included the control variable opportunity to donate, which is the number of trials where the subject could have fed another bat (see electronic supplementary material). The distribution of residuals did not deviate from normal (Shapiro Wilk’s test: W = 0.98, p = 0.95). To visualize results, we plotted mean food received against residual past sharing to nonkin females—the residuals from a regression of the number of unrelated females fed on number of opportunities to donate (to control for the latter).

3. Results

Under typical conditions, when key donors were present, the number of female nonkin fed in previous years did not predict the amount of food received; instead the trend was negative (figure 1a;R2= 0.43, β = −52.4, t = −1.81, p = 0.155). However, feeding more female nonkin did predict receiving more food later when a female’s key donor was absent (figure 1b;R2 = 0.56, β = 56.0, t = 3.68, p = 0.004). A bat’s proclivity to invest in female nonkin therefore predicted the change in total food she received when key donors were removed (R2 = 0.58, F2,11 = 7.54; β = 108.4, t = 3.48, p = 0.005; figure 1c). Females that fed more female nonkin coped better with partner removal. This result was robust to several variations in the analysis (see electronic supplementary material).

fig1bl
Figure 1.
Bats with a higher propensity to help unrelated females suffered smaller losses in total food received when a key donor was removed as a potential donor. Proclivity to feed more nonkin females (x-axis) did not positively correlate with food received when a non-donor was absent (a) but it did when the key donor was absent (b). Feeding more unrelated females predicted smaller reductions in food received when the key donor was removed (c). Shading shows 95% CI of the slope.

4. Discussion

Our results support the social bet-hedging hypothesis. By helping nonkin, individuals appear to maintain a wider support network than would be possible through only helping close kin. This suggests that female vampire bats can reduce the costs of losing a key donor by ‘not putting all their eggs in one basket’.

The social bet-hedging hypothesis makes three key assumptions. First, it assumes that individuals shift cooperative investments to and from individuals based on their relative cooperative returns, as predicted by reciprocity and biological market theory (e.g. models of partner control and partner choice) [1–3].

Second, it assumes not only that there are fitness benefits to having both more cooperative partners and stronger relationships [11–17], but also that individuals often face a trade-off between investing in relationship quantity versus quality (strength). If cooperative relationships require continuous investment, then merely increasing the number of weak connections can reduce overall cooperative returns, just as increasing offspring production at the expense of offspring quality does not reliably increase fitness [18]. On the other hand, strengthening each relationship can come at the expense of relationship quantity, so individuals might therefore divert investments towards partners that yield lower indirect fitness or reciprocal returns simply to create more relationships.

Third, social bet-hedging only makes sense if lost cooperative partnerships cannot be replaced instantly and effortlessly (as evidenced by figure 1a). Backup partners must already be in place. Social bet-hedging therefore assumes that new relationships require time and energy to develop. This seems true for food-sharing vampire bats [5–10].

Social bet-hedging may also exist for other cooperative behaviours. For example, female baboons increase their social grooming rates and groom more partners after the death of a close female relative [19], suggesting that investments in more relationships can help to compensate for the loss of a key social partner. In humans, although relationship quality is better than relationship quantity at predicting received social support [20], people appear to benefit from a greater number of weaker friendships in environments where friends are more likely to leave [21].

Many models of cooperation focus on pairwise interactions (e.g. [2]), but cooperative ‘exchange rates’ are determined by the supply and demand of cooperative services and partners—properties of the larger social network [22]. Many cooperative species might allocate cooperative investments across several partners and compare the varying return rates from each [3,22]. It remains unclear, however, if or how different social animals balance the quality and quantity of social ties. By influencing the number and strength of connections in a social network, strategies like social bet-hedging can both shape, and be shaped by, social network structure.

Ethics: All procedures were approved by the University of Maryland Institutional Animal Care and Use Committee (Protocol R-10-63).

Data accessibility: The data supporting this article have been uploaded as part of the electronic supplementary material.

Authors’ contributions: G.G.C. and D.R.F. conceived the analysis, G.G.C. carried out the analysis, and D.R.F. and G.S.W. advised the analysis. G.G.C. drafted the manuscript; D.R.F. and G.S.W. revised it critically for important intellectual content. All authors gave final approval of the version to be published, and agree to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Funding: Work by G.G.C. was supported by a Ford Predoctoral Fellowship, a Dissertation Improvement Grant from the National Science Foundation (IOS-1311336), and grants from the American Society of Mammalogists and Animal Behavior Society.

Acknowledgements: We thank the Organization for Bat Conservation for their extraordinary support. Ronald Noë, Rachel Crisp, Julia Vrtilek and two anonymous reviewers provided comments that improved the manuscript.

References

  • [1] Trivers, R.L. 1971 The evolution of reciprocal altruism. Quarterly Review of Biology. 46, 35-57.
  • [2] Axelrod, R. & Hamilton, W.D. 1981 The evolution of cooperation. Science 211, 1390-1396.
  • [3] Noë, R. & Hammerstein, P. 1994 Biological markets: supply and demand determine the effect of partner choice in cooperation, mutualism and mating. Behavioral Ecology and Sociobiology 35, 1-11.
  • [4] Philippi, T. & Seger, J. 1989 Hedging one’s evolutionary bets, revisited. Trends in Ecology & Evolution 4, 41-44.
  • [5] Carter, G.G. & Wilkinson, G.S. 2013 Food sharing in vampire bats: reciprocal help predicts donations more than relatedness or harassment. Proceedings of the Royal Society of London B 280, 20122573.
  • [6] Carter, G.G. & Wilkinson, G.S. 2015 Social benefits of non-kin food sharing by female vampire bats. Proceedings of the Royal Society of London B 282, 20152524-20152524.
  • [7] Wilkinson, G.S. 1984 Reciprocal food sharing in the vampire bat. Nature 308, 181-184.
  • [8] Carter, G.G. & Wilkinson, G. 2013 Does food sharing in vampire bats demonstrate reciprocity? Communicative and Integrative Biology 6, e25783. (doi:10.4161/cib.25783).
  • [9] Wilkinson, G.S. 1988 Reciprocal altruism in bats and other mammals. Ethology and Sociobiology 9, 85-100.
  • [10] Wilkinson, G.S. 1985 The social organization of the common vampire bat: I. Pattern and cause of association. Behavioral Ecology and Sociobiology 17, 111-121.
  • [11] Kokko, H., Johnstone, R.A. & Clutton-Brock, T.H. 2001 The evolution of cooperative breeding through group augmentation. Proceedings of the Royal Society of London B 268, 187-196.
  • [12] Seyfarth, R.M. & Cheney, D.L. 1984 Grooming, alliances and reciprocal altruism in vervet monkeys. Nature 308, 541-543.
  • [13] Seyfarth, R.M. & Cheney, D.L. 2012 The evolutionary origins of friendship. Annual Review of Psychology 63, 153-177.
  • [14] Seyfarth, R.M., Silk, J.B. & Cheney, D.L. 2014 Social bonds in female baboons: the interaction between personality, kinship and rank. Animal Behaviour 87, 23-29.
  • [15] Silk, J.B., Beehner, J.C., Bergman, T.J., Crockford, C., Engh, A.L., Moscovice, L.R., Wittig, R.M., Seyfarth, R.M. & Cheney, D.L. 2009 The benefits of social capital: close social bonds among female baboons enhance offspring survival. Proceedings of the Royal Society of London B 276, 3099-3104.
  • [16] Silk, J.B., Beehner, J.C., Bergman, T.J., Crockford, C., Engh, A.L., Moscovice, L.R., Wittig, R.M., Seyfarth, R.M. & Cheney, D.L. 2010 Strong and consistent social bonds enhance the longevity of female baboons. Current Biology 20, 1359-1361.
  • [17] Wittig, R.M., Crockford, C., Lehmann, J., Whitten, P.L., Seyfarth, R.M. & Cheney, D.L. 2008 Focused grooming networks and stress alleviation in wild female baboons. Hormones and Behavior 54, 170-177.
  • [18] Smith, C.C. & Fretwell, S.D. 1974 The optimal balance between size and number of offspring. The American Naturalist 108, 499-506.
  • [19] Fruteau, C., Voelkl, B., van Damme, E. & Noë, R. 2009 Supply and demand determine the market value of food providers in wild vervet monkeys. Proceedings of the National Academy of Sciences USA 106, 12007-12012.
  • [20] Engh, A.L., Beehner, J.C., Bergman, T.J., Whitten, P.L., Hoffmeier, R.R., Seyfarth, R.M. & Cheney, D.L. 2006 Behavioural and hormonal responses to predation in female chacma baboons (Papio hamadryas ursinus). Proceedings of the Royal Society of London B 273, 707-712.
  • [21] Franks, H.M., Cronan, T.A. & Oliver, K. 2004 Social support in women with fibromyalgia: Is quality more important than quantity? Journal of Community Psychology 32, 425-438.
  • [22] Oishi, S. & Kesebir, S. 2012 Optimal social-networking strategy is a function of socioeconomic conditions. Psychological Science, 0956797612446708.

Text Supplement

Supplement to methods

For each female test subject, we selected a unique key donor. All targeted key donor pairs were symmetrical such that if bat A was the key donor for bat B, then B was the targeted key donor for A. This was possible because if bat A was one of the most frequent donors for B, then B was typically one of the most frequent donors for A. The key donor was the subject’s highest-ranking donor, i.e. the bat that gave it the most food, in nine cases (including three mothers, four daughters, another relative, and one nonrelative). The key donor was the subject’s the second-highest-ranking donor in four cases (including one mother, another relative, and two nonrelatives). However, in one case (one nonrelative), the key donor was the highest-ranking recipient for the subject, but only the ninth-highest-ranking donor. In each trial, a possible donor was excluded by either removing it or fasting it on the same night, and this occurred on five occasions separated by at least 7 days.

The control variable opportunity to donate explained 79% of the variation in the observed number of partners fed (F(1,13)=48, p<0.0001), and it also predicted the number of nonkin females fed (R2=0.31, F(1,13)=5.5, p=0.038). Opportunity to donate was determined by a bat’s presence or absence in the home cage during past fasting trials, which was influenced by age (Spearman’s correlation with age: 0.58; p=0.03) and the bat being haphazardly excluded from some past fasting trials based on sickness, injury, or recent birth of a pup.

Supplement to results

When controlling for opportunity to donate, the effect of the number of nonkin females fed on the change in food received remained the same after excluding three cases where key donors failed to donate (R2=0.64, n=11, F(2,8)=7.1, nonkin females fed: beta=115.5, t=3.16, p=0.0134). The effect was also detected when using nonkin females fed per opportunity to donate as the predictor (R2=0.29, n=14, F=4.79, p=0.0490). When we added key donor kinship as a factor (kin or nonkin) and the interaction between kinship and nonkin females fed as predictors in the model, we found no interaction effect (p=0.73). When this interaction term was removed, we found that nonkin females fed (beta=108.2, t=3.30, p=0.008), but not kinship (p=0.95), predicted the change in food received.

Supplement to discussion

Social bet-hedging can be seen as a strategy for balancing two potentially contradicting strategies: group augmentation, defined as investing in group members to increase group size, i.e. partner quantity (Kokko et al. 2001, Kingma et al. 2014), and reciprocity, defined as investing preferentially in specific partners that provide the best reciprocal returns, i.e. partner quality (Trivers 1971, Carter 2014). Imagine you are the ideal Darwinian primate, deciding how much to groom each member of your group to maximize cooperative returns and hence inclusive fitness. For simplicity in this case, assume all kinship is equal. Each groupmate will later provide you with food, if you have groomed them sufficiently, and each group member might differ in the amount of food they would feed you per unit of grooming received. Assume that return rates are tracked by some form of emotional scorekeeping, and that you therefore have full knowledge of which relationships provide the greatest return rates, assuming those individuals are present. There are countless ways to divide your time and energy. You could spend 100% of your grooming effort on your best food provider. You could allocate 85% to her and 10% to the next best and 5% to the third best. You could split your grooming effort equally among all group members. It’s easy to see the analogy with betting or financial investing. The optimal strategy will depend on the distribution of food-sharing probabilities and amounts (Kelly 1956). If one partner provides the highest return rate, then you should simply invest everything in that partner, i.e. a partner choice strategy. On the other hand, if all groupmates are equally likely to provide food and to provide equal amounts of food, then you should simply maximize the number of partners that are alive or available to you, i.e. group augmentation. However, if partner return rates or availability vary over time, then “social bet-hedging” becomes relevant.

The need for social bet-hedging also depends on the timescale of reciprocal relationship formation: how much grooming does it take to create a relationship that starts benefiting you with food sharing? If social grooming can immediately lead to food sharing in the next minute, then social bet-hedging is not necessary, because when food is needed, you can immediately divert social grooming to the current best partner. If, however, a food-sharing relationship requires several days of previous grooming investment, then you should already be grooming many different partners, in case they can become future food providers in a time of need. This form of social bet-hedging requires long-term contingency embedded within complex, stable, multi-benefit relationships, so it is most likely to be found in primate or primate-like societies composed of stable individualized cooperative relationships. It would be particularly interesting to test the extent to which subconscious decisions to invest in relationship quantity or quality influence human social networks of collaboration or friendship.

Supplement references

  • Carter GG. 2014. The reciprocity controversy. Animal Behavior and Cognition 1:368-386.
  • Kelly JL. 1956. A new interpretation of information rate. Bell System Technical Journal 35:917-926.
  • Kingma SA, Santema P, Taborsky M, and Komdeur J. 2014. Group augmentation and the evolution of cooperation. Trends in Ecology and Evolution 29:476-484.
  • Kokko H, Johnstone RA, and Clutton-Brock TH. 2001. The evolution of cooperative breeding through group augmentation. Proceedings of Royal Society London B 268:187-196.
  • Trivers RL. 1971. The evolution of reciprocal altruism. Quarterly Review of Biology 46:35-57.
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Latest paper: Reproductive seasonality, sex ratio and philopatry in Argentina’s common vampire bats

It can be found here.

Summary:

  • 35 years of field observations
  • 13,642 mist-net captures and 181 whole roost captures
  • vampire bats in Argentina (near the southern limit of their range) have a reproductive season (unlike most other places)
  • we have new records for oldest wild vampire bats: 16 and 17 years
  • we corroborated prior evidence of male-biased dispersal and female philopatry
  • once settled in a location, adults of both sexes can spend years and perhaps their lifetime at the same site
  • despite frequent disturbance, vampire bats readily roosted in man-made structures
  • males feed earlier in the night
  • males visit female roosts at night (returning to their own roosts by day), but females also visit male roosts
  • 82% of vampires captured in mist nets were in the bottom half near the ground
  • we found evidence of a consistent male-biased sex ratio even among newborns and mature fetuses (reason unknown!)
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A new field site in Panama

I am hoping to develop some new long-term field sites for future work on vampire bats.

On March 27, I traveled with Austin Garrido, Rob Mies (director of the Organization for Bat Conservation), his daughter Georgia Mies, and labmates May Dixon, Rachel Crisp, Katharina Eggert, Hugo Narizano, and Julia Vrtilek to Lake Bayano, a two-hour drive from our lab in Gamboa, Panama. This is closer than our other field site which is five hours away. On a previous trip, I had seen several stable roosting groups of vampire bats (Desmodus rotundus) in Pueblo Nuevo Cave along with other bats including Natalus mexicanus roosting individually, Carollia perspicillata roosting in small groups, and large mixed aggregations of Pteronotus gymnonotus and, I think, Pteronotus parnelli.

We saw the same species on this trip. At least 3-4 female groups of vampire bats were located in the first part of the cave that is easily accessible from the entrance. These are groups I hope to track in the future using proximity loggers. See the video below with high-definition infrared footage shot by Rob Mies, which allowed me to count the bats.

There are apparently about five cattle pastures in the surrounding area. That night, during the new moon, we set mist-nets around corralled cattle at the closest pasture hoping to catch and band a sample of vampire bats and perhaps even see some of those same marked individuals back in the cave. A large mark-recapture study could even help us estimate the vampire bat population size.

That night, we caught only 25 vampires bats in our nets. Three escaped from the hand or net being before being processed (a female and two bats of unknown sex). Interestingly, only 5 of 24 vampire bats we netted at the cattle pasture were female. One of these female vampires was a yearling, not fully grown. The captures were spread pretty evenly throughout the night, but the highest density of captures seemed to be between 1:45 and 4:00 am. We recaptured two of the bats we banded. The last bat we caught was around 4:30 am and we took down nets around 5 am.

The next day, I saw one of the banded males back in the cave. The three original female groups were still there. Hopefully, this will be a second site that Simon Ripperger and I will study social foraging in vampire bats. I had valuable discussions with the cattle farmers. They agreed to gather the farmers together at some point when we return in order to discuss what work we would like to do there in the future.

A big special thanks to Austin Garrido for organizing logistics, to May Dixon for help with all-night mist-netting, and to Rob Mies for footage.

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Update: three golden opportunities

Now – October 2017, the Smithsonian Institute has awarded me with a fellowship to finish collecting data from lab and field experiments on vampire bat social behavior with Rachel Page at the Smithsonian Tropical Research Institute in Panama.

November 2017 – August 2018, the Humboldt Foundation has awarded me a fellowship to learn more about social network analysis, resampling methods, and simulations in collaboration with Damien Farine at the Department of Collective Behavior, Max Planck Institute for Ornithology, in Germany.

August 2018, I will be back in the USA working in the Department of Evolution, Ecology and Organismal Biology at The Ohio State University as a tenure-track assistant professor of biology. I will also continue my collaborations with the Organization for Bat Conservation.

This is an exciting time, and the challenge for me is to make the very most of it! I find myself in the unbelievably fortunate and privileged position of being gifted the freedom to do what I love, and given the resources to do it as well as I can. For this, I owe a tremendous debt of gratitude to my recent mentors, Jerry Wilkinson, John Ratcliffe, and Rachel Page. Most of all, I thank everyone on Team Vampire.

Work as hard as much as you want to on the things you like to do the best. Don’t think about what you want to be, but what you want to do!Richard Feynman

 

 

 

 

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Reciprocity before Trivers

“New” ideas are rarely new. In science we stand on the shoulders of giants and whenever I read the works of the giants, I often find that many ideas or discoveries– that I thought were “mine” or belonged to some more recent author– were actually first described by Darwin or some other author from long ago.

I hope to soon publish a paper on a hypothesis I call “social bet-hedging” which is the idea that individuals might face a trade-off between investing in the quantity versus quality (strength) of cooperative relationships, and that, in unpredictable social environments having more friendships might be better than  investing in fewer stronger friendships (even if the opposite is true normally). More on this in a future blogpost.

Before publishing it, I looked through the cooperation literature and emailed people who have most influenced me on the topic of cooperative relationships: Ronald Noe, Dorothy Cheney, and Robert Seyfarth. I wanted to make sure that I had not accidentally stolen the idea from someone else.

If you read the scientific literature on a given topic in backwards chronological order, you find that authors with new ideas tend to overemphasize their originality. This is probably also true for novel technology. In science, most “new ideas” are really incremental developments or novel applications of older ideas. Work that is labeled “transformative” and “revolutionary” often involves taking something that’s been around awhile (but never fully appreciated) and showing its general importance in a convincing manner.

Even when new ideas are truly new, they often are built on a foundation that allows contemporary thinks to converge of the same new idea. For example, before Darwin famously discovered natural selection, some forester you probably never heard of named Patrick Matthew discovered it three decades earlier. He compared artificial selection on trees with what normally happens in a forest: the healthiest most fecund trees survive and reproduce (kinda obvious really). He wrote,

“There is a law universal in nature, tending to render every reproductive being the best possibly suited to its condition that its kind, or that organized matter, is susceptible of, which appears intended to model the physical and mental or instinctive powers, to their highest perfection, and to continue them so. This law sustains the lion in his strength, the hare in her swiftness, and the fox in his wiles. As Nature, in all her modifications of life, has a power of increase far beyond what is needed to supply the place of what falls by Time’s decay, those individuals who possess not the requisite strength, swiftness, hardihood, or cunning, fall prematurely without reproducing—either a prey to their natural devourers, or sinking under disease, generally induced by want of nourishment, their place being occupied by the more perfect of their own kind, who are pressing on the means of subsistence.”

That first sentence is not the best example of clear writing, but that was the style back then in ye olde days. Even more unfortunate is that he published this in an appendix to a book entitled Naval Timber and Arboriculture (1831) where it remained mostly unread.

As Ernst Mayr summarized:

Patrick Matthew undoubtedly had the right idea, just like Darwin did on September 28, 1838, but he did not devote the next twenty years to converting it into a cogent theory of evolution. As a result it had no impact whatsoever.

Not everyone thinks this is fair. Yep, there’s a full conspiracy theory regarding this “greatest cover-up in the history of science”.

The double invention of calculus is another example of new ideas coming about independently but simultaneously, giving the impression that the time was ripe and the stage was set.

New ideas never jump into existence fully formed by single people. They are memes that persist by being passed along (like natural selection), and they evolve by branching off from previous forms (like speciation). For this reason, most discoveries come into focus gradually. True “Eureka” moments in science are rare. Profound new idea are always built on foundation of less appreciated past work.

I was reminded of this recently while reading a section of the classic work Adaptation and Natural Selection by GC Williams (1966). So many of the ideas I attributed to Trivers’s notion of “reciprocal altruism” (1971) and its application to human friendship could be traced back to older works, even well-read classics like this one.

Before I present the key text, I’ll recap a bit of brief background. The concept of reciprocal altruism or reciprocity was formulated by Trivers 1971 (Quarterly Review of Biology) with the suggestion that each individual’s need to enforce mutual benefit could help explain many behaviors that underlie enduring cooperative relationships, including human friendship. The idea was extremely influential.

Trivers’ paper also touched upon on almost every related topic, such that for every subsequent extension of Trivers’ idea, one can find a mention of it in his original paper. For instance, biological market theory (Noe and Hammerstein 1994, 1995) later added the role of market effects and the emphasized a distinction between models of partner choice and partner control (i.e. reciprocal altruism). But in his paper, Trivers’ mentioned the role partner choice in friendship. He also described cases where cooperation was enforced by ecological circumstance rather than by behavior (now called “pseudoreciprocity” or “byproduct benefits”). He described applications to cleaner-client fish, which later became an important model system. Trivers also mentioned the iterated prisoner’s dilemma as a model for the evolution of reciprocity, which was later formalized by Axelrod & Hamilton ten years later (1981 Science). He even mentioned interactions between reciprocity and kinship which have only been experimentally explored recently. Although Trivers never actually worked on reciprocity himself, he at least mentioned almost all the new ideas and directions that would be developed from his theory.

As a term, “reciprocal altruism” is competing with other terms and concepts in the struggle for existence. In biology, the popularity of this term (and the breadth of its definition) rose to a peak in the 1990s, where it became mired in confusion and controversy, eventually falling in popularity until today it is defined very specifically and often considered unimportant outside of humans. I wrote a review explaining how and why this happened.

But I digress. My point here is that the foundations for the concept of reciprocity had already been floating around in the collective scientific consciousness before Trivers (1971). For example, the “tit-for-tat” demonstration built upon the ‘folk theorem’ of game theory–that repeating interactions which influence fitness can stabilize the evolution of almost any behavioral trait through social reward/punishment–an observation that has been understood since the 1950s.

A second example: here is the text from GC Williams Adaptation and Natural Selection: A Critique of Some Current Evolutionary Thought (1966) discussing contingency in cooperative relationships (bold emphasis mine).

…I wish to consider an apparent exception to the rule that the natural selection of individuals cannot produce group-related adaptations. This exception may be found in animals that live in stable social groups and have the intelligence and other mental qualities necessary to form a system of personal friendships and animosities that transcend the limits of family relationship. Human society would be impossible without the ability of each of us to know, individually, a variety of neighbors. We learn that Mr. X is a noble gentleman and that Mr. Y is a scoundrel. A moment of reflection should convince anyone that these relationships may have much to do with evolutionary success. Primitive man lived in a world in which stable interactions of personalities were very much a part of his ecological environment. He had to adjust to this set of ecological factors as well as to any other. If he was socially acceptable, some of his neighbors might bring food to himself and his family when he was temporarily incapacitated by disease or injury. In time of dearth, a stronger neighbor might rob our primitive man of food, but the neighbor would be more likely to rob a detestable primitive Mr. Y and his troublesome family. Conversely, when a poor Mr. X is sick our primitive man will, if he can, provide for him. Mr. X’s warm heart will know the emotion of gratitude and, since he recognizes his benefactor and remembers the help provided, will probably reciprocate some day. A number of people, including Darwin (1896, Chap. 5), have recognized the importance of this factor in human evolution. Darwin speaks of it as the “lowly motive” of helping others in the hope of future repayment. I see no reason why a conscious motive need be involved. It is necessary that help provided to others be occasionally reciprocated if it is to be favored by natural selection. It is not necessary that either the giver or the receiver be aware of this.

Simply stated, an individual who maximizes his friendships and minimizes his antagonisms will have an evolutionary advantage, and selection should favor those characters that promote the optimization of personal relationships. I imagine that this evolutionary factor has increased man’s capacity for altruism and compassion and has tempered his ethically less acceptable heritage of sexual and predatory aggressiveness. There is theoretically no limit to the extent and complexity of group-related behavior that this factor could produce, and the immediate goal of such behavior would always be the well-being of some other individual, often genetically unrelated. Ultimately, however, this would not be an adaptation for group benefit. It would be developed by the differential survival of individuals and would be designed for the perpetuation of the genes of the individual providing the benefit to another. It would involve only such immediate self-sacrifice for which the probability of later repayment would be sufficient justification. The natural selection of alternative alleles can foster the production of individuals willing to sacrifice their lives for their offspring, but never for mere friends.

The prerequisites for the operation of this evolutionary factor are such as to confine it to a minor fraction of the Earth’s biota. Many animals form dominance hierarchies, but these are not sufficient to produce an evolutionary advantage in mutual aid. A consistent interaction pattern between hens in a barnyard is adequately explained without postulating emotional bonds between individuals. One hen reacts to another on the basis of the social releasers that are displayed, and if individual recognition is operative, it merely adjusts the behavior towards another individual according to the immediate results of past interactions. There is no reason to believe that a hen can harbor grudges against or feel friendship toward another hen. Certainly the repayment of favors would be out of the question.

A competition for social goodwill cannot fail to have been a factor in human evolution, and I would expect that it would operate in many of the other primates. Altman (1962) described the formation of semipermanent coalitions between individuals within bands of wild rhesus monkeys and cited similar examples from other primates. Members of such coalitions helped each other in conflicts and indulged in other kinds of mutual aid. Surely an individual that had a better than average ability to form such coalitions would have an evolutionary advantage over its competitors. Perhaps this evolutionary factor might operate in the evolution of porpoises. This seems to be the most likely explanation for the very solicitous behavior that they sometimes show toward each other (Slijper, 1962, pp. 193-197). I would be reluctant, however, to recognize this factor in any group but the mammalia, and I would imagine it to be confined to a minority of this group. For the overwhelming mass of the Earth’s biota, friendship and hate are not parts of the ecological environment, and the only way for socially beneficial self-sacrifice to evolve is through the biased survival and extinction of populations, not by selective gene substitution within populations.


The observation that great new ideas often have precedents can also be made about Hamilton’s inclusive fitness theory, the best contender for most important and influential theory in social evolution. This idea, which Maynard Smith later renamed “kin selection”, was supposedly discussed informally by JBS Haldane in the 1950s.

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Maynard Smith’s apology letter in the magazine New Scientist for taking credit away from WD Hamilton and assigning it to JBS Haldane

Most people agree that the credit for the idea of kin selection must go to Hamilton. But some people attribute it to Haldane or Maynard-Smith, and much worse, I have seen many lay authors and social scientists credit the famous author Richard Dawkins with these ideas, because he popularized it in his classic 1976 book “The Selfish Gene”. For better or worse, the evolutionary success of a new idea will depend not only on its accuracy, but its ability to be understood and to thereby influence others. This is why Dawkins did more for spreading Hamilton’s ideas than Hamilton did. Credit typically goes to those who do the best job of developing and explaining the ideas’ importance to others and making it available for them to use. And sometimes the jobs of innovation, development, and popularization are best done by different people.

Scientists are motivated by getting recognition for their work, but perhaps we scientists should be explicit that we should (and do) give less credit to whoever had the idea first. If you have a good idea, there’s a good chance someone else had it first. What matters more is what you do with your ideas. The most important reason to know everything relevant that came before is to advance knowledge or develop it further without wasting time reinventing the wheel.

Posted in About cooperation, About science as an activity | Leave a comment

Field notes on weekend trip to Costa Rica (with disc-winged bats!)

Spix’s disc-winged bat Thyroptera tricolor has suction cups (yes, suction cups) on its thumbs, and it uses these to cling to the smooth surface of young, furled Heliconia leaves.

I’ve wanted to see a disc-winged bat since I was about ten years old, and I finally got to see them this week while visiting Gloriana Chaverri, and Caroline and Michael Schöner at their field site in Costa Rica over the weekend.

Gloriana is a leading expert on social lives of Neotropical leaf-dwelling bats. This includes bats that chew leaves to make them into “tents” as well as disc-winged bats (Thyroptera). Over the last seven years, Gloriana has shown that Thyroptera live in small groups with multiple matrilines that often switch between their very temporary roosts, the furled leaves [1-3]. Both sons and daughters often remain at their natal site, and inbreeding is avoided because the bats mate with members of other populations. Each population includes several groups that switch among several roosts.

Despite moving daily between their tubular leaf roosts, the bats maintain very cohesive social networks. To coordinate their roost-switching, the bats use a system of contact calling [4-7]. Bats flying in search of their group make one contact call type called an “inquiry call” and groupmates within furled leaves make another call type in response. The calls have both individual and group-level signatures. The calls are also amplified by the funnel-like shape of the leaf roost.

Here’s a video of one flying into a leaf roost:

 

Most recently, Gloriana has been working with Caroline and Michael Schöner. The Schöners have pioneered work on an astonishing mutualism in another leaf-dwelling bat [8-10]. There is a pitcher plant in the paleotropics (Nepenthes) that has coevolved with a small insectivorous bat of the genus Kerivoula. The bat lives inside the pitcher and defecates into the fluid-filled “pitcher”. Most pitcher plants are carnivorous. They trap, drown, and digest insects inside the tiny pool of their pitcher, but this pitcher plant is modified to be a tiny little one-bat house. The level of the digestive fluid is lower to accommodate the bat’s roosting position. The plant lets the bat do the capturing, chewing, and pre-digesting of the insect prey. Some pitcher plants also attract shrews with a nectar reward and get them to poop into the pitcher [11]. For lack of a more polite term, the Schöners call the plants “coprophagous”.

In exchange for nutrients, the plant benefits the bat by providing it with a literal “roof over it’s head” and it’s distinctive shape is acoustically attractive to the bats. This is yet another example of bat-plant acoustic communication. There are also bat-pollinated flowers and leaves that reflect and enhance the echolocation calls of bats when they are ready to be pollinated [12-13].

What’s especially intriguing is that Kerivoula will also live in a different pitcher plant species that is not coevolved for the bats, and the bats can only fit inside the pitcher because it has been emptied. How? Something chews a small hole at the base of the pitcher to drain the liquid out. Could it be the bat? Nobody knows for sure. The Schöners suspect this is the case, but they have not yet caught the bat in the act. The bat might be a mutualist for the first species, but a parasite for the other. Or perhaps there’s a three-way interaction: the bat, the pitcher plant, and a third mystery organism that makes the hole, perhaps to drinks the pitcher plant liquid. It’s an unsolved mystery.

See also this blogpost by Merlin Tuttle and photos.

The Schöners are surprised by the physical similarities of Thyroptera and Kerivoula, although the personalities of the two bats are quite distinct. Kerivoula will eat larger insects and has the bite to match. Thyroptera it seems are a bit easier to work with. After your experiments are done, you can release Thyroptera into a furled leaf and they will just crawl inside and stay. As Caroline puts it, “Thyroptera is more well-behaved.”

The Schöners are tracking the bats’ movements among different leaves in the wild. Do the same bats consistently find new leaves and others follow? Or do all the bats do a search on their own? They are also looking at the bats use of spatial memory when relocating roosts. For this experiment, they work in a flight tent with an array of artificial leaves. The work is fascinating and I’m excited to see the results.

The Schöners take turns tromping around in the forest looking for bats and staying at the field station looking after their 9-month-old, Sophia, who loves fried platanos and has inherited the Schöners’ love of smiling. One similarity between Gloriana and the Schöners is their friendliness and propensity for hearty laughing. The atmosphere at the field station is one of joyful cheer, with everyone trying their best to make Sophie smile. It’s been a great place for a holiday.

Before coming to the Baru field station where I am now, I visited two caves with my wife Michelle, my labmate Nia Toshkova, and our guide: Gloriana’s graduate student Stanimira Deleva, who is studying the variation in use of caves by all different Costa Rican bats. The larger caves was two kilometers long and full of Pteronotus gymnonotus or Pternotus davyi. The smaller cave had Saccopteryx bilineata and Peropteryx kappleri. Nia and Stanimira are old friends, both cavers from Bulgaria. Michelle and I met Stanimira on a caving trip in Panama where I found a new potential site to work with vampire bats.

Here is a video of the Thyroptera being very cute:

References:

  1. Chaverri, G., & Kunz, T. H. (2011). All-offspring natal philopatry in a neotropical bat. Animal behaviour, 82(5), 1127-1133.
  2. Buchalski M, Chaverri G, and Vonhof M. 2014. When genes move farther than offspring: gene flow by male gamete dispersal in the highly philopatric bat species Thyroptera tricolor. Molecular Ecology 23:464-480.
  3. Chaverri G. 2010. Comparative social network analysis in a leaf-roosting bat. Behavioral Ecology and Sociobiology 64:1619-1630.
  4. Chaverri G, Gillam EH, and Vonhof MJ. 2010. Social calls used by a leaf-roosting bat to signal location. Biology Letters 6:441-444.
  5. Gillam EH, and Chaverri G. 2012. Strong individual signatures and weaker group signatures in contact calls of Spix’s disc-winged bat, Thyroptera tricolor. Animal Behaviour 83:269-276.
  6. Chaverri G, Gillam EH, and Kunz TH. 2012. A call-and-response system facilitates group cohesion among disc-winged bats. Behavioral Ecology 24:481-487.
  7. Chaverri G, and Gillam EH. 2013. Sound amplification by means of a horn-like roosting structure in Spix’s disc-winged bat. Proceedings of the Royal Society B 280:20132362.
  8. Grafe TU, Schöner CR, Kerth G, Junaidi A, and Schöner MG. 2011. A novel resource–service mutualism between bats and pitcher plants. Biology Letters 7:436-439.
  9. Schöner CR, Schöner MG, Kerth G, and Grafe TU. 2013. Supply determines demand: influence of partner quality and quantity on the interactions between bats and pitcher plants. Oecologia 173:191-202.
  10. Schöner MG, Schöner CR, Simon R, Grafe TU, Puechmaille SJ, Ji LL, and Kerth G. 2015. Bats are acoustically attracted to mutualistic carnivorous plants. Current Biology 25:1911-1916.
  11. Clarke, C. M., Bauer, U., Ch’ien, C. L., Tuen, A. A., Rembold, K., & Moran, J. A. (2009). Tree shrew lavatories: a novel nitrogen sequestration strategy in a tropical pitcher plant. Biology Letters, 5(5), 632-635.
  12. von Helversen, D., & von Helversen, O. (1999). Acoustic guide in bat-pollinated flower. Nature, 398(6730), 759-760.
  13. Simon, R., Holderied, M. W., Koch, C. U., & von Helversen, O. (2011). Floral acoustics: conspicuous echoes of a dish-shaped leaf attract bat pollinators. Science, 333(6042), 631-633.
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New paper: risk exaggerates nepotism in vampire bats

Here’s the paper.

In evolutionary biology, we often draw a line between “altruism” and other cooperative traits. Altruistic traits are special in that they lead to a net cost to one’s survival and reproduction. Some traits are clear cases: when a bee stings you it dies, so the suicidal bee sting is an altruistic trait.

But nature abhors clear categories. Most seemingly “altruistic” behaviors are ambiguous in whether they pose net average fitness benefits or costs. This leads to some confusion for several reasons. First, most acts that most people call altruistic are not altruism in the evolutionary sense. Any form of “reciprocal altruism” is not really altruism as defined above. This is why people who study animal cognition invented the term “prosocial” behavior to avoid the word “altruism” and all the inevitable semantic arguments with evolutionary biologists. Second, the kinds of costs we can easily measure (like time and energy) are not the same as fitness costs which can only be measured after whole lifetimes have gone by, so this means we can’t categorize most of the cooperative behaviors that we are studying. Third, many people equate helping kin with “altruism” but much helping between kin might actually be mutually beneficial. For example, natural selection might have shaped me to care about the survival of my family, not just because that helps them survive, but also because it helps my own survival.

For traits like this that pose both costs and benefits to the helper (food sharing in vampire bats is an example), it’s better to think of there being a spectrum where the exact cost/benefit ratios of a cooperative trait can slide around from positive to negative depending on the circumstances. It’s not a completely different behavior just because you move from -0.1 to +0.1 direct fitness effects.

Thankfully, to better understand a cooperative trait, we don’t always need to try to unambiguously classify traits or exactly measure the change in lifetime reproductive success that comes from performing the behavior. Instead, we can just change the factor we think is important and see if the animal’s helping decisions also changes as one would expect from theory. Rather than measuring lifetime fitness consequences, we can test the design of the trait. In this case, what information is involved the decision-making process?

For example, many animal parents will go to extreme lengths to protect their babies (e.g. below is footage of a mother moose attacking a truck) and various theories (inclusive fitness and parent-offspring conflict) makes predictions about the design of this behavior.

A mother’s brain should be designed by natural selection to put herself at some degree of risk to save her offspring, but not too much risk. Unlike the sterile worker bee, she is not a genetic dead-end, so she should not carelessly cast away her own life for any potential benefit to her genetic kin. Theory predicts that at some risk to her own survival and reproduction, she should give up on trying to save her offspring. There’s a risk factor that can be tuned up and down that should have an effect on the probability of A helping B, and this factor should interact with genetic relatedness. One could also tune up the kinship factor. As the famous quote by Haldane goes: I would give up my life to save 2 brothers or 8 cousins.

Risk should decrease my willingness to help and increase the degree to which I care about someone’s relatedness to me. As you dial down the risk, I am more willing to help: I would not run into a burning building, suffering certain third degree burns, to help a total stranger, but I would do it if I had protective gear. As you dial up the risk to me, the circle of people I would be willing to help in that situation should shrink: I would jump in the ocean to save a stranger, but I would only jump in shark-infested waters to save my child.

Like other animals, we don’t weigh the costs and benefits consciously, but the emotional urgency we feel to help or not help depends on situation-based cues that have, in our evolutionary past, acted as reliable indicators of inclusive fitness benefits of helping in situations similar to the one we are facing. 

So how can we test this in food-sharing vampire bats?

A few years ago, I was trying to record contact calls from hungry vampire bats. So put a caged hungry bat in a larger flight room with the other bats and put a microphone on it. I discovered to my surprise that other bats would feed these trapped individuals through the cage bars. At some point, this gave me the idea to do a small side experiment to test the idea that idea that risk increases nepotism.

To manipulate the perceived risks of helping, I created a novel “rescue” condition, where any donor vampire bat had to leave her warm, safe, dark, and comfy roosting location alongside her groupmates, then descend to an illuminated spot (vampire bats are very light phobic) where the trapped bat was stuck, and then to feed the trapped bat, she has to press her face to the cage bars (which sometimes makes her surroundings invisible) and regurgitate across cage bars. Compared to normal food-sharing, they don’t seem to like doing this. But they do it.

Sixteen of 29 bats were fed by others when trapped. They were fed by both kin and nonkin, but the degree of nonkin sharing declined quite obviously. All 15 starved bats that were tested in both trapped and free conditions received less food when trapped, and they received a consistently greater proportion of this food from closer relatives when trapped than when free. The vampires were more willing to feed mothers, daughters, and sons in the rescue condition. This is what we should expect if the bats’ nepotistic biases are exaggerated under dangerous conditions.

This paper was published in the journal Behavioral Ecology. Or if you lack institutional access you can get it from me here.

 

 

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