Evolutionary Biology

Mutualisms-cooperative interactions among different species-are known to influence global biodiversity. Nevertheless, theoretical and empirical work has led to divergent hypotheses about how mutualisms modulate diversity. We ask here when and how mutualisms influence species richness. Our synthesis suggests that mutualisms can promote or restrict species richness depending on mutualist function, the level of partner dependence, and the specificity of the partnership. These characteristics, which themselves are influenced by environmental and geographic variables, regulate species richness at different scales by modulating speciation, extinction, and community coexistence. Understanding the relative impact of these mechanisms on species richness will require the integration of new phylogenetic comparative models as well as the manipulation and monitoring of experimental communities and their resulting interaction networks. Mutualisms and Species Richness: An Ecological and Evolutionary Conundrum Mutualisms-cooperative interactions among different species-are ubiquitous, have shaped much of global biodiversity, and have allowed organisms to access or outsource crucial functions such as transport, nutrition, cleaning, and defense. A large body of research has suggested strong links between mutualisms and the generation and maintenance of species diversity on Earth. However, this suite of hypotheses is complex, spans multiple scales, and can at times be contradictory. For example, at the ecological scale, May [1] argued that mutualisms have no effects on species diversity within communities. He argued that, because negative density-dependence (see Glossary) favors the coexistence of multiple species, mutualisms-which are associated with positive density-dependence-should do the opposite. This was later contrasted by newer empirical and theoretical studies highlighting asymmetry in the effects of mutualisms and suggesting that the formation of mutualistic networks plays a key role in promoting coexistence among multiple species [2-4]. The debate continues, with some researchers suggesting that species interactions including mutualisms play little role in shaping evolution [5], and that partnerships tend to stabilize species rather than promoting their diversification [6]. By contrast, a growing body of work claims the opposite, namely that mutualistic partnerships are an integral driver of morphological and evolutionary diversification [7-9]. In this review we ask when and how mutualisms influence diversity. Instead of including other metrics of diversity, we specifically focus on species richness to simplify our approach. Because this topic is so broad, we focus on two major areas of research. In the first we address how mutualisms impact lineage diversification rates, and in the second we examine how mutualisms impact on community coexistence, focusing on the modulation of competition dynamics. Highlights There are contrasting hypotheses about the influence of mutualisms on species richness. We provide a synthetic framework for how mutualisms influence species richness at the ecological and evolutionary scales. Mutualisms can promote or restrict species richness depending on their function, level of dependence, and specificity. Because the outcomes of mutualisms are highly dependent on environmental variables, we forecast that the effects of mutualisms on species richness are also strongly influenced by biotic, abiotic, and geographic variables across ecological and evolutionary timescales. Although our review depicts the complex and multifaceted impact of mutu-alisms on species richness, it also highlights a key gap: our understanding of the relative importance of the mechanisms through which mutual-isms affect biodiversity. We suggest new methodological approaches to fill this gap.