Differential effects of nematode infection on pollinating and non-pollinating fig wasps: Can shared antagonism provide net benefits to a mutualism?

Species pairs that form mutualistic associations are also components of broader organismal community networks. These interaction networks have shaped the evolution of individual mutualisms through interspecific interactions ranging from secondarily mutualistic to intensely antagonistic. Our understanding of this complex context remains limited because characterizing the impacts of species interacting with focal mutualists is often difficult. How is the fitness of mutualists impacted by the co-occurring interactive network of community associates? We investigated this context using a model interaction network comprised of a fig and fig wasp mutualist, eight non-pollinating fig wasp (NPFW) antagonists/commensals and a nematode previously believed to be associated only with the pollinator wasp mutualist. Through repeated sampling and field observations, we characterized the ecological roles of these mutualist-associated organisms to identify key antagonists. We then investigated how potential nematode infection of NPFWs could impact wasp survival across key life stages and, in turn, inferred how this influences the fitness of the fig-pollinator mutualists. Unexpectedly, we found all Ficus petiolaris-associated NPFWs to be the targets for nematode infection, with infection levels sometimes exceeding that of pollinators. Experimental data collected for the most abundant NPFW species suggest that nematode infection significantly reduces their longevity. Further, comparisons of nematode loads for emerging and successfully arriving NPFWs suggest that infection severely limits their dispersal ability. Through these observations, we conclude that this infection could impact NPFWs more severely than either mutualistic partner, suggesting a novel role of density-dependent facultative mutualism between figs, pollinator wasps and the nematode. This antagonist-mediated suppression of other network antagonists may present an ecologically common mechanism through which antagonists can present net benefits for mutualists' fitness.

Multi-locus phylogenies of the genus Barteria (Passifloraceae) portray complex patterns in the evolution of myrmecophytism.

The four species of the central African genus Barteria show variation in habitat and in degree of association with ants. Whereas B. solida, restricted to submontane forests, attracts opportunistic ants to extrafloral nectar, the three other species, found in lowland rainforests (B. fistulosa, B. dewevrei) and in littoral scrub (B. nigritana), possess stem domatia of varying shapes and degrees of specialisation, hosting either non-specific arboreal ants (B. nigritana, some B. dewevrei) or two large species of ants of the genus Tetraponera Smith, 1852 that are specific to some species of Barteria (B. fistulosa, some B. dewevrei). We aimed to investigate whether this variation represents an evolutionary trend toward increasing specialisation of mutualism or the reduction or loss of myrmecophytic traits. For this, we determined phylogenetic relationships within the genus using DNA sequences (primarily nuclear ITS) and microsatellite genotypes (11 loci) on a large sample of individuals, mostly from Cameroon and Gabon. The two types of markers support an initial dichotomy that groups B. dewevrei with B. nigritana and B. fistulosa with B. solida respectively. Within these pairs, species do not appear reciprocally monophyletic. At microsatellite loci, B. nigritana forms a clade embedded within B. dewevrei; and within both B. solida and B. fistulosa, geographical populations show levels of differentiation similar to that observed between populations of B. solida and B. fistulosa. Geographic distance alone does not account for genetic differentiation between species, which indicates reproductive isolation. Divergence in each of the two pairs implies evolutionary transitions in habitat and in myrmecophytism. Specialised mutualism with specific ant species of the genus Tetraponera has been lost in species found in more marginal habitats.