Does the evolution of ontogenetic niche shifts favour species coexistence? An empirical test in Trinidadian streams.

A major question in ecology is how often competing species evolve to reduce competitive interactions and facilitate coexistence. One untested route for a reduction in competitive interactions is through ontogenetic changes in the trophic niche of one or more of the interacting species. In such cases, theory predicts that two species can coexist if the weaker competitor changes its resource niche to a greater degree with increased body size than the superior competitor. We tested this prediction using stable isotopes that yield information about the trophic position (δ15 N) and carbon source (δ13 C) of two coexisting fish species: Trinidadian guppies Poecilia reticulata and killifish Rivulus hartii. We examined fish from locations representing three natural community types: (1) where killifish and guppies live with predators, (2) where killifish and guppies live without predators and (3) where killifish are the only fish species. We also examined killifish from communities in which we had introduced guppies, providing a temporal sequence of the community changes following the transition from a killifish only to a killifish-guppy community. We found that killifish, which are the weaker competitor, had a much larger ontogenetic niche shift in trophic position than guppies in the community where competition is most intense (killifish-guppy only). This result is consistent with theory for size-structured populations, which predicts that these results should lead to stable coexistence of the two species. Comparisons with other communities containing guppies, killifish and predators and ones where killifish live by themselves revealed that these results are caused primarily by a loss of ontogenetic niche changes in guppies, even though they are the stronger competitor. Comparisons of these natural communities with communities in which guppies were translocated into sites containing only killifish showed that the experimental communities were intermediate between the natural killifish-guppy community and the killifish-guppy-predator community, suggesting contemporary evolution in these ontogenetic trophic differences. These results provide comparative evidence for ontogenetic niche shifts in contributing to species coexistence and comparative and experimental evidence for evolutionary or plastic changes in ontogenetic niche shifts following the formation of new communities.

The evolution of size-dependent competitive interactions promotes species coexistence.

Theory indicates that competing species coexist in a community when intraspecific competition is stronger than interspecific competition. When body size determines the outcome of competitive interactions between individuals, coexistence depends also on how resource use and the ability to compete for these resources change with body size. Testing coexistence theory in size-structured communities, therefore, requires disentangling the effects of size-dependent competitive abilities and niche shifts. Here, we tested the hypothesis that the evolution of species- and size-dependent competitive asymmetries increased the likelihood of coexistence between interacting species. We experimentally estimated the effects of size-dependent competitive interactions on somatic growth rates of two interacting fish species, Trinidadian guppies Poecilia reticulata and killifish Rivulus hartii. We controlled for the effects of size-dependent changes in the niche at two competitive settings representing the early (allopatric) and late (sympatric) evolutionary stages of a killifish-guppy community. We fitted the growth data to a model that incorporates species- and size-dependent competitive asymmetries to test whether changes in the competitive interactions across sizes increased the likelihood of species coexistence from allopatry to sympatry. We found that guppies are competitively superior to killifish but were less so in sympatric populations. The decrease in the effects of interspecific competition on the fitness of killifish and increase in the interspecific effect on guppies' fitness increased the likelihood that sympatric guppies and killifish will coexist. However, while the competitive asymmetries between the species changed consistently between allopatry and sympatry between drainages, the magnitude of the size-dependent competitive asymmetries varied between drainages. These results demonstrate the importance of integrating evolution and trait-based interactions into the research on how species coexist.

Fifty years of capacity building in the search for new marine natural products.

The Convention on Biological Diversity, and the Nagoya Protocol in particular, provide a framework for the fair and equitable sharing of benefits arising from the utilization of biological resources and traditional knowledge, and ultimately aim to promote capacity-building in the developing world. However, measuring capacity-building is a challenging task due to its intangible nature. By compiling and analyzing a database of scientific peer-reviewed publications over a period of 50 y (1965 to 2015), we investigated capacity-building in global marine natural product discovery. We used publication and authorship metrics to assess how the capacity to become scientifically proficient, prolific, and independent has changed in bioprospecting countries. Our results show that marine bioprospecting is a dynamically growing field of research with continuously increasing numbers of participating countries, publications, and scientists. Yet despite longstanding efforts to promote equitability and scientific independence, not all countries have similarly increased their capacity to explore marine biodiversity within their national jurisdiction areas. Although developing countries show an increasing trend in the number of publications, a few developed countries still account for almost one-half of all publications in the field. Multiple lines of evidence suggest that economic capacity affects how well countries with species-rich marine ecosystems can scientifically explore those resources. Overall, the capacity-building data analyzed here provides a timely contribution to the ongoing international debate about access to and benefit-sharing of biological resources for countries exploring biodiversity within and outside their national jurisdiction areas.

An experimental test of how parasites of predators can influence trophic cascades and ecosystem functioning.

Parasites can shape the structure and function of ecosystems by influencing both the density and traits of their hosts. Such changes in ecosystems are particularly likely when the host is a predator that mediates the dynamics of trophic cascades. Here, we experimentally tested how parasite load of a small predatory fish, the threespine stickleback, can affect the occurrence and strength of trophic cascades and ecosystem functioning. In a factorial mesocosm experiment, we manipulated the density of stickleback (low vs. high), and the level of parasite load (natural vs. reduced). In addition, we used two stickleback populations from different lineages: an eastern European lineage with a more pelagic phenotype (Lake Constance) and a western European lineage with a more benthic phenotype (Lake Geneva). We found that stickleback caused trophic cascades in the pelagic but not the benthic food chain. Evidence for pelagic trophic cascades was stronger in treatments where parasite load of stickleback was reduced with an antihelmintic medication, and where fish originated from Lake Constance (i.e., the more pelagic lineage). A structural equation model revealed that differences in stickleback lineage and parasite load were most likely to impact trophic cascades via changes in the composition, rather than overall biomass, of zooplankton communities. Overall, our results provide experimental evidence that parasites of predators can influence the cascading effects of fish on lower trophic levels with consequences on ecosystem functioning.

Transgenerational selection driven by divergent ecological impacts of hybridizing lineages.

Dynamic interactions between ecological conditions and the phenotypic composition of populations likely play an important role in evolution, but the direction and strength of these feedbacks remain difficult to characterize. We investigated these dynamics across two generations of threespine sticklebacks from two evolutionary lineages undergoing secondary contact and hybridization. Independently manipulating the density and lineage of adults in experimental mesocosms led to contrasting ecosystem conditions with strong effects on total survival in a subsequent generation of juveniles. Ecosystem modifications by adults also varied the strength of selection on competing hybrid and non-hybrid juveniles. This variation in selection indicated (1) a negative eco-evolutionary feedback driven by lineage-specific resource depletion and dependence and (2) a large performance advantage of hybrid juveniles in depleted environments. This work illustrates the importance of interactions between phenotype, population density and the environment in shaping selection and evolutionary trajectories, especially in the context of range expansion with secondary contact and hybridization.

Trophic and stoichiometric consequences of nutrification for the intertidal tropical zoanthid Zoanthus sociatus.

Zoanthids are conspicuous and abundant members of intertidal environments, where they are exposed to large environmental fluctuations and subject to increasing loads of anthropogenic nutrients. Here we assess the trophic ecology and stoichiometric consequences of nutrient loading for symbiotic zoanthids inhabiting different intertidal habitats. More specifically, we analysed the stable isotope signature (δ13C and δ15N), elemental composition (C, N and P) and stoichiometry (C:N, C:P, N:P) of Zoanthus sociatus differently exposed to nutrification. Results suggest that autotrophy is the main feeding mode of zoanthids and that the effect water nutrient content differently affects the elemental phenotype of zoanthids depending on tidal habitat. Additionally, habitat effects on Z. sociatus P-related stoichiometric traits highlight functional differences likely associated with variation in Symbiodinium density. These findings provide an innovative approach to assess how cnidarian-dinoflagellate symbioses response to ecosystem changes in environmentally dynamic reef flats, particularly nutrient loading.

Experimental evidence that parasites drive eco-evolutionary feedbacks.

Host resistance to parasites is a rapidly evolving trait that can influence how hosts modify ecosystems. Eco-evolutionary feedbacks may develop if the ecosystem effects of host resistance influence selection on subsequent host generations. In a mesocosm experiment, using a recently diverged (<100 generations) pair of lake and stream three-spined sticklebacks, we tested how experimental exposure to a common fish parasite (Gyrodactylus spp.) affects interactions between hosts and their ecosystems in two environmental conditions (low and high nutrients). In both environments, we found that stream sticklebacks were more resistant to Gyrodactylus and had different gene expression profiles than lake sticklebacks. This differential infection led to contrasting effects of sticklebacks on a broad range of ecosystem properties, including zooplankton community structure and nutrient cycling. These ecosystem modifications affected the survival, body condition, and gene expression profiles of a subsequent fish generation. In particular, lake juvenile fish suffered increased mortality in ecosystems previously modified by lake adults, whereas stream fish showed decreased body condition in stream fish-modified ecosystems. Parasites reinforced selection against lake juveniles in lake fish-modified ecosystems, but only under oligotrophic conditions. Overall, our results highlight the overlapping timescales and the interplay of host-parasite and host-ecosystem interactions. We provide experimental evidence that parasites influence host-mediated effects on ecosystems and, thereby, change the likelihood and strength of eco-evolutionary feedbacks.

The association of feeding behaviour with the resistance and tolerance to parasites in recently diverged sticklebacks.

Divergent natural selection regimes can contribute to adaptive population divergence, but can be sensitive to human-mediated environmental change. Nutrient loading of aquatic ecosystems, for example, might modify selection pressures by altering the abundance and distribution of resources and the prevalence and infectivity of parasites. Here, we used a mesocosm experiment to test for interactive effects of nutrient loading and parasitism on host condition and feeding ecology. Specifically, we investigated whether the common fish parasite Gyrodactylus sp. differentially affected recently diverged lake and stream ecotypes of three-spined stickleback (Gasterosteus aculeatus). We found that the stream ecotype had a higher resistance to Gyrodactylus sp. infections than the lake ecotype, and that both ecotypes experienced a cost of parasitism, indicated by negative relationships between parasite load and both stomach fullness and body condition. Overall, our results suggest that in the early stages of adaptive population divergence of hosts, parasites can affect host resistance, body condition and diet.

Kinship reinforces cooperative predator inspection in a cichlid fish.

Kin selection theory predicts that cooperation is facilitated between genetic relatives, as by cooperating with kin an individual might increase its inclusive fitness. Although numerous theoretical papers support Hamilton's inclusive fitness theory, experimental evidence is still underrepresented, in particular in noncooperative breeders. Cooperative predator inspection is one of the most intriguing antipredator strategies, as it implies high costs on inspectors. During an inspection event, one or more individuals leave the safety of a group and approach a potential predator to gather information about the current predation risk. We investigated the effect of genetic relatedness on cooperative predator inspection in juveniles of the cichlid fish Pelvicachromis taeniatus, a species in which juveniles live in shoals under natural conditions. We show that relatedness significantly influenced predator inspection behaviour with kin dyads being significantly more cooperative. Thus, our results indicate a higher disposition for cooperative antipredator behaviour among kin as predicted by kin selection theory.

Social deprivation affects cooperative predator inspection in a cichlid fish.

The social environment individuals are exposed to during ontogeny shapes social skills and social competence in group-living animals. Consequently, social deprivation has serious effects on behaviour and development in animals but little is known about its impact on cooperation. In this study, we examined the effect of social environment on cooperative predator inspection. Predator inspection behaviour is a complex behaviour, which is present in a variety of shoaling fish species. Often, two fish leave the safety of the group and inspect a potentially dangerous predator in order to gather information about the current predation risk. As predator inspection is highly risky, it is prone to conflicts and cheating. However, cooperation among individuals may reduce the individual predation risk. We investigated this complex social behaviour in juveniles of the cichlid fish Pelvicachromis taeniatus that were reared in two different social environments throughout development. Fish reared in a group inspected more often than isolation-reared fish and were more likely to cooperate, i.e. they conducted conjoint inspection of a predator. By contrast, isolation-reared fish were more likely to perform a single inspection without a companion. These results suggest an impairment of cooperative behaviour in isolation-reared fish most probably due to lack of social experience and resulting in lowered social skills needed in coordinated behaviour.