Behavioral ecology, Sociobiology, Evolutionary game theory, Biogeography
Major Research Achievements (2013-2017)
- I have used an integrative approach that includes behavioral observations, experimental manipulations, and evolutionary theoretical modeling, to study the ecological and social determinants of social evolution and the ecological consequences of sociality. I will describe some of my key findings in the following sections.
- 1. The ecology of social evolution
- Identifying the factors that modulate cooperative and competitive behaviors is the key to understanding social evolution. However, how ecological factors affect social conflict and their fitness consequences remain poorly explored. I used both a game-theoretical model and empirical data to show that Taiwan yuhinas (Yuhina brunneiceps)—a joint-nesting species in which group members are unrelated—employ more cooperative strategies in unfavorable environmental conditions (Shen et al. 2012). Fighting duration became shorter, a smaller total number of eggs were laid, and incubation was more likely to start after all females completed egg laying (which led to more synchronous egg hatching). Surprisingly, as a consequence, there were more surviving offspring under unfavorable conditions because the cooperative strategy resulted in fewer dead nestlings. To our knowledge, this study is the first theoretical analysis and an empirical study demonstrating that an unfavorable environment reduces social conflict, resulting in better fitness consequences in social vertebrates.
- Featured article in Nature Communications (Shen et al. 2012)
- 2. Evolution of cooperative breeding
- Most social animals cooperate with kin because the genetic interests between relatives are more aligned for kin than for non-kin. The formation of non-kin groups thus stands as a strange exception and can help us achieve a more general understanding of social evolution. I study the evolution of non-kin groups in Taiwan yuhinas. We found most yuhinas formed groups with non-kin (Liu et al. 2015). However, kin were more likely than non-kin to be accepted in the groups when group sizes are larger than the most productive sizes. Based on the study of yuhinas, I have also developed a general theory of the evolution of cooperative social groups (Shen et al. 2016, Shen et al. 2014, Reeve and Shen 2013).
- Previous theories on cooperative breeding have largely focused on the evolution of offspring delayed dispersal, in which mature offspring stay at their natal territories. In such “helper-at-the-nest” type cooperative breeding groups, per capita productivity often decreases as group size increases. Thus, the primary benefit for offspring to stay is to access the resources of their natal territories. On the other hand, in species like yuhinas, there is often an optimal group size, which suggests that there are benefits generated by cooperation. We apply the insider-outsider conflict model, simultaneously considering the interests of current group members and potential joiners, to demonstrate that non-kin groups are more likely to form when cooperation benefits are significant, whereas if resource access benefits are important, relatives should more likely be tolerated. Studying the evolution of non-kin cooperation can help us understand the general principle of stable cooperation.
- Our study is the only study in Asian appearing on the either versions of cooperative breeding books.
- 3. Ecological consequences of sociality
- Social animals, including humans and social insects, have come to dominate the land environment of the earth, possibly because of their ability to form complex societies. However, the ecological consequences of sociality, such as the niche breadth and ecological dominance of a species, have received surprisingly little attention. Here we study the evolution of thermal generalists and specialists in the cooperatively breeding burying beetle (Nicrophorus nepalensis) by examining the costs and benefits of grouping along an elevational gradient, where the intensity of temperature-mediated interspecific competition for carcasses decreases with increasing elevation (Sun et al. 2014). By manipulating the group size along an elevational gradient and recording their investment and competing behaviors, we found that large groups performed as thermal generalists and small groups as thermal specialists. This intriguing generalist-specialist tradeoff along the thermal and elevational gradients in N. nepalensis is caused by the conflict between individual’s self-interest and group wellbeing. Our study shows that in the unfavorable lower-elevation environment, where the pressure of competition with flies is highest, individuals in large groups not only were more cooperative in handling carcasses but also engaged at lower levels of social conflict, enabling them to outcompete flies. We also experimentally heated carcasses to determine the role of temperature in shaping the cooperation and conflict in burying beetles in cooler environments (above 2000m), where solitary breeders performed better. We found that heating carcasses significantly lowered the breeding success of small groups but not large groups. This provides direct evidence that the benefit of cooperation is to cope with the stronger interspecific competition pressure in hotter environments. Examining the ecological consequences of cooperation may help us not only to understand why so many of the social insects have conquered the earth but also to determine how climate change will affect the success of these and other social species, including our own species.
- This paper (Sun et al. 2014) is highlighted by eLife.
- 4. Climatic variability and species range size
- Understanding how species adapt physiologically to variable environments has crucial implications for conservation, as climatic variability shifts with global climate change. The climatic variability hypothesis (CVH) posits that the scope of climatic variability increases with latitude or elevation and that greater variability selects for organisms with broader tolerances, enabling them to become geographically more widespread. Although CVH appears to be a widely accepted macrophysiological principle, the implications of climatic variability for this hypothesis at different temporal scales have not been investigated. In a comprehensive analytical framework, we test the classical hypothesis for elevational range sizes of more than 16,500 terrestrial vertebrate species. In support of CVH, mean elevational range size is positively correlated with seasonal temperature range (STR), but we found a negative relationship between range size and diurnal temperature range (DTR), indicating that physiological specialization may be favored under shorter-term variability. Our empirical findings are in accord with Gilchrist’s phenotypic optimality model and with our extended version of it, which incorporates a more general form of environmental variability. We further showed that the mean annual precipitation (MAP) gradient, rather than latitude, plays a key role in influencing the relative relationship of DTR and STR to the species range size. We conclude that the interplay between longer-term and shorter-term climatic variability shapes the evolution of environmental generalists and specialists.
- 1. Combined Effects of Habitat Alteration and Elevation Influence Species Competitive Interactions through Changing Climatic Variability
- By studying burying beetles’ social behavior in the field, we notice that they are very sensitive to the environmental change. Thus, we also design experiments to understand the influences of habitat alteration on beetle’s breeding success along the elevational gradient. Habitat alternation is one of the most important drivers of global biodiversity loss. A possible moderating factor is microclimate experienced by species. Tropical insects are thought to have narrower thermal tolerance range due to adaptation for stable thermal environment. Whether such a narrower thermal tolerance range leads insects more sensitive to microclimatic changes under habitat alteration is therefore a crucial question. We investigated breeding performance of burying beetles (Nicrophorus nepalensis) between cultivated lands and natural forests and along elevational gradient. We found that diurnal variation in air temperature is critical for their breeding success. Habitat type predominantly modified daily maximum air temperature (ATmax) on the basis of the gradient of daily minimum air temperature (ATmin) along elevation. Probability of breeding success was significantly lower in cultivated lands than in natural forests, which was well explained by larger daily temperature range (DTRair). The effect of DTRair was also confirmed in manipulative experiments in laboratory. Our results demonstrate that habitat alteration leads to microclimate change independent of the effect of altitudinal lapse and subsequently modify the thermal environment species actual experienced. Thermal specialists in tropical mountains are venerable to the negative impacts of increasing short-term climatic variability resulted from habitat alteration.
- 2. Habitat alteration, Allee effect and range size in burying beetles
- Based on our field study, we found an interesting pattern that lower distribution boundaries are surprisingly different between east and west populations of N. nepalensis: In the east, the habitats are mostly protected by the national park and are nature forests. The lower boundary of N. nepalensis’ distribution range is 1200 m in the summer. Whereas in the west, most habitats are modified as farms and ranches, the lower limit of beetles’ distribution range is about 1650 m. We have measured the microclimate of nature forests in both east- and west- sides of central mountain and there were no significant differences between the two. But, we still could not find any beetles in the fragmented nature forests in the west, although when we experimentally brought beetles to form groups and bred in these lower forests, they still can successfully breed. Thus, we hypothesize that Allee effect, which states that in some species, individual fitness at low population numbers shows positive density dependence: the greater their number, the better their fitness, could be the mechanism causing the differences of range limits between the east and west populations. We will thus measure the population density and using our breeding box, as used in our social behavior studies, to studies how N. nepalensis’ fitness is influenced by the population and habitat alteration, which, in term, might influence their geographic distribution range sizes.
- 3. Sociogenomics of cooperation and conflict in burying beetles
- It is well-known that carcass size and nest failure rate are the main ecological factors influencing the costs and benefits of grouping in burying beetles. However, we found, interestingly, that individuals only cooperatively buried carcass and provisioned young with the presence of competition of flies, regardless of the resource size. We have further discovered that N. nepalensis‘ cooperative behavior can be induced by dimethyl sulfide (DMS), which is the volatile emitted after fly maggots digesting the carcass. We believe this is the first study demonstrating that a single chemical can induce animal’s cooperative behavior, which results in forming cooperative breeding groups. Based this exciting finding of a simple “switch” of their cooperative behavior, we want to further understand the genetic mechanisms of cooperative social behaviors in N. nepalensis. In collaborating with Dr. Wen-Hsiung Li, Dr. Jason Tsai, and Dr. John Wang, we plan to conduct the following research. First, we will identify olfactory receptor genes responsible for the DMS perception by sequencing the transcriptome of antennae. Second, we will quantify the variations of cooperative behavior within species by quantifying aggressiveness of individuals. Our preliminary results showed that in about 80% of DMS treated cases, individuals formed cooperative breeding groups. While in the other 20% of cases, the dominant individuals remained highly aggressive in defending the carcass, which resulted in single female or a pair monopolizing the carcass. This result suggested that there is likely a genetic variation in aggressiveness in N. nepalensis. Third, we will identify “cooperative genes” by comparing genetic background of individuals showing most or least aggressive behavior. A genome-wide approach will be applied to identify cooperative genes by screening genetic markers tightly linked to the candidate genes.
- Wang, H.-Y.*, Y.-S. Chen, C.-C. Hsu, and S.-F. Shen, 2017, “Fishing-induced changes in adult length are mediated by skipped-spawning”, ECOLOGICAL APPLICATIONS, 27(1),274-284. (SCI) (IF: 4.252; SCI ranking: 11.6%,16%)
- Chan, W.-P. , I-C. Chen, R. K. Colwell, W.-C. Liu, C.-y. Huang, S.-F. Shen*, 2016, “Seasonal and daily climate variation have opposite effects on species elevational range size”, SCIENCE, 351(6280), 1427-1439. (SCI) (IF: 34.661; SCI ranking: 3.2%)
- Safran RJ, Scordato ES, Wilkins MR, Hubbard JK, Jenkins BR, Albrecht T, Flaxman SM, Karaardic H, Vortman Y, Lotem A, Nosil P, Pap P, Shen S, Chan SF, Parchman TL, Kane NC, 2016, “Genome-wide differentiation in closely related populations: the roles of selection and geographic isolation.”, Molecular ecology, 25(16), 3865-3883. (SCI) (IF: 5.947; SCI ranking: 12.1%,7.3%,10.9%)
- Liu, M., Q.-D. Zhong, S.-H. Li, S. Fang, C.-E. Pu, H.-W. Yuan*, S.-F. Shen*, 2015, “The genetic relatedness in groups of joint-nesting Taiwan yuhinas: low genetic relatedness with preferences for male kin”, PLoS One, 10(6): e0127341. (SCI) (IF: 3.057; SCI ranking: 17.5%)
- Sun, S.-J., D. R. Rubenstein, B.-F. Chen, S.-F. Chan, J.-N. Liu, M. Liu, W. Hwang, P.-S. Yang, S.-F. Shen*, 2014, “Climate-mediated Cooperation Promotes Niche Expansion in Burying Beetles”, eLife, 3, e02440. (SCI) (IF: 8.282; SCI ranking: 4.7%)
- Shen S.-F.*, E. Akcay, D. R. Rubenstein, 2014, “Group size and social conflict in complex societies”, AMERICAN NATURALIST, 183 (2), 301-310. (SCI) (IF: 3.148; SCI ranking: 39.1%,27.3%)
- Reeve, H. K.*†, S.-F., Shen†, 2013, “Unity and disunity in the search for a unified reproductive skew theory”, ANIMAL BEHAVIOUR, 85(6), 1137-1144. (SCI) (IF: 3.169; SCI ranking: 23.5%,5%)
- Chan, W.-P. , H.-W.Yuan, C.-Y. Huang, C.-H. Wang, S.-D. Lin, Y.-C. Lo, B.-W. Huang, K. A. Hatch, H.-J. Shiu, C.-F. You, Y.-M*. Chang and S.-F. Shen* , 2012, “Regional scale high resolution δ18O prediction in precipitation using MODIS EVI”, PLoS One, 7(9), e45496. (SCI) (IF: 3.057; SCI ranking: 17.5%)
- Shen, S.-F.*, S. L. Vehrencamp, R. A. Johnstone, H.- C. Chen, S.-F. Chan, W.-Y. Liao, K.-Y. Lin and H.-W. Yuan*. , 2012, “Unfavorable environment limits social in Yuhina brunneiceps”, Nature Communications, 3, 885. (SCI) (IF: 11.329; SCI ranking: 4.8%)
- Shen, S.-F.*, H. K. Reeve, S. L. Vehrencamp, 2011, “Parental care, costly young and reproductive skew: A general model of parental investment in cooperatively breeding societies”, Journal of Theoretical Biology, 284 (1), 24-31. (SCI) (IF: 2.049; SCI ranking: 29.1%,25%)
- Shen, S.-F., H. K. Reeve*, and W. Herrnkind, 2010, “The brave leader game and the timing of altruism among non-kin”, American Naturalist, 176(2), 242-248. (SCI) (IF: 3.148; SCI ranking: 39.1%,27.3%)
- Shen, S.-F., H.- C. Chen, S. L. Vehrencamp, and H.-W. Yuan* , 2010, “Group provisioning limits sharing conflict among nestlings in joint-nesting Taiwan yuhinas.”, Biology Letters, 6, 318-321. (SCI) (IF: 2.823; SCI ranking: 31.3%,47.8%,22.1%)
- Shen, S.-F. and H. K. Reeve* , 2010, “Reproductive skew theory unified: the general bordered tug-of-war model.”, Journal of Theoretical Biology, 263(1), 1-12. (SCI) (IF: 2.049; SCI ranking: 29.1%,25%)
- Shen, S.-F. and H. K. Reeve. 2010. Reproductive skew. p.p 54-58. In Encyclopedia of Animal Behavior . (M. Breed, eds). NY: Academic Press
Rubenstein, D.R. and S.-F. Shen.2009 Reproductive conflict and the costs of social status in cooperatively breeding vertebrates. The American Naturalist 173:650-661 (SCI) (IF: 4.796; ranking: 8.7%)
Cant, M. A. and S.-F. Shen. 2006. Endogenous timing in competitive interactions among relatives. Proceedings of Royal Society, London Series B. 273:171-178 (SCI) (IF: 4.857; ranking: 8%)
Reeve, H. K. and S.-F. Shen. 2006. A missing model, the boarded tug-of-war of reproductive skew. PNAS 103: 8430–8434 (SCI) (IF: 9.432; ranking: 6.2%)