Phylogeny versus body size as determinants of food web structure Russell E. Naisbit 1, † , Rudolf P. Rohr 1, †, ‡ , Axel G. Rossberg 2, } , Patrik Kehrli 1, k and Louis-Fe ´lix Bersier 1, * 1 Unit of Ecology and Evolution, Department of Biology, University of Fribourg, Chemin du Muse ´e 10, 1700 Fribourg, Switzerland 2 School of Biological Sciences, Medical Biology Centre, Queen’s University Belfast, 97 Lisburn Road, Belfast BT9 7BL, UK Food webs are the complex networks of trophic interactions that stoke the metabolic fires of life. To under- stand what structures these interactions in natural communities, ecologists have developed simple models to capture their main architectural features. However, apparently realistic food webs can be generated by models invoking either predator –prey body-size hierarchies or evolutionary constraints as structuring mechanisms. As a result, this approach has not conclusively revealed which factors are the most important. Here we cut to the heart of this debate by directly comparing the influence of phylogeny and body size on food web architecture. Using data from 13 food webs compiled by direct observation, we confirm the importance of both factors. Nevertheless, phylogeny dominates in most networks. Moreover, path analysis reveals that the size-independent direct effect of phylogeny on trophic structure typically outweighs the indirect effect that could be captured by considering body size alone. Furthermore, the phylogenetic signal is asymmetric: closely related species overlap in their set of consumers far more than in their set of resources. This is at odds with several food web models, which take only the view-point of consumers when assigning interactions. The echo of evolutionary history clearly resonates through current food webs, with implications for our theoretical models and conservation priorities. Keywords: body mass; ecological network; food web; path analysis; phylogenetic constraints; trophic structure 1. INTRODUCTION Faced with the diversity of feeding interactions in nature, from the rapid strike of a great white shark to the patient trapping of a web-spinning spider, a search for general patterns appears a daunting task. Yet, these are precisely the generalities we should identify to construct realistic models of trophic networks, with the goal of understand- ing how they evolve, what allows such complex systems to remain stable and how we might conserve them in the face of species loss, invasion or climate change. It is broadly accepted that trophic interactions are (given the habitat) predominantly controlled by traits of consumer and resource. The most intuitive is body size, which is easily measured for almost all species and clearly delimits the range of resources that a consumer can feasi- bly and profitably tackle ([1], p. 59, [2 – 5]). However, the structure of trophic interactions arises from a multitude of other factors, and systematically identifying these traits is difficult. Phylogeny provides a useful surrogate for this information, as closely related species typically share many trophically relevant traits and consequently occupy similar trophic niches [6 – 8]. These two obser- vations have led to two research paradigms as to what predominantly determines trophic interactions: ‘body size’ and ‘phylogeny’. While these two mechanisms are obviously not mutually exclusive, most models of food web structure have focused on one of these two factors as a source of inspiration for designing simple rules for who eats whom within a community. For example, the cascade [9] and niche models [10] assign feeding links between species according to a hierarchy that is often assumed to represent body size, while the nested hierarchy [6] and matching models [11] illustrate how phylogeny might influence trophic structure in a community. The quality of early models was assessed by generating many model food webs and summarizing them using a variety of descriptive statistics, such as the proportion of basal species or the mean food chain length [12,13]. More recently formu- lated models allow direct comparisons with observed food webs, on the basis of the number of links that are cor- rectly fitted or using likelihood [3,14 – 18]. However, because these models typically consider only the influence of either one or the other factor, the contributions of body size and phylogeny have never been explicitly compared. Here, we turn directly to the food web data to ask, which is the stronger predictor of trophic structure— phylogeny or body size? * Author for correspondence: (louis-felix.bersier@unifr.ch). † These authors contributed equally to the study. ‡ Present address: Integrative Ecology Group, Estacio ´n Biolo ´gica de Don ˜ana (EBD–CSIC), C/Ame ´rico Vespucio s/n, 41092, Sevilla, Spain. } Present address: Lowestoft Laboratory, Centre for Environment, Fisheries and Aquaculture Science (CEFAS), Pakefield Road, Lowestoft, Suffolk NR33 0HT, UK. k Present address: Station de Recherche Agroscope Changins- Wa ¨denswil, 1260 Nyon, Switzerland. Electronic supplementary material is available at http://dx.doi.org/ 10.1098/rspb.2012.0327 or via http://rspb.royalsocietypublishing.org. Proc. R. Soc. B (2012) 279, 3291–3297 doi:10.1098/rspb.2012.0327 Published online 23 May 2012 Received 13 February 2012 Accepted 2 May 2012 3291 This journal is q 2012 The Royal Society on July 11, 2012 rspb.royalsocietypublishing.org Downloaded from