Interactions among plants and evolution

We examined the linkage between climate and interspecific plant interactions in New England salt marshes. Because harsh edaphic conditions in marshes can be ameliorated by neighboring plants, plant neighbors can have net competitive or facilitative interactions, depending on ambient physical stresses. In particular, high soil salinities, which are largely controlled by solar radiation and the evaporation of marsh porewater, can be ameliorated by plant neighbors under stressful conditions leading to facilitative interactions. Under less stressful edaphic conditions, these same neighbors may be competitors. In this paper, we use this mechanistic understanding of marsh plant interactions to examine the hypothesis that latitudinal and inter-annual variation in climate can influence the nature and strength of marsh plant species interactions. We quantified the relationship between climate and species interactions by transplanting marsh plants into ambient vegetation and unvegetated bare patches at sites north and south of Cape Cod, a major biogeographic barrier on the east coast of North America. We hypothesized that the cooler climate north of Cape Cod would lead to fewer positive interactions among marsh plants. We found both latitudinal and inter-annual variation in the neighbor relations of marsh plants that paralleled latitudinal differences in temperature and salinity. South of Cape Cod, plant neighbor interactions tended to be more facilitative, whereas north of Cape Cod, plant neighbor interactions were more competitive. At all sites, soil salinity increased and plant neighbor interactions were more facilitative in warmer versus cooler years. Our results show that interspecific interactions can be strikingly linked to climate, but also reveal that because the sensitivity of specific species interactions to climatic variation is highly variable, predicting how entire communities will respond to climate change will be difficult, even in relatively simple, well-studied systems.

Coevolutionary dynamics in host–parasite systems are shaped by reciprocal selection and environmental context. When hosts and parasites share ancestry and ecological overlap, selection can act on similar traits, but population structure and geography may generate adaptive mosaics. Here, we present the first study to investigate genome-wide signatures of selection in response to a broad climatic gradient and a geographic mosaic of coevolution between a social parasite and its host. We examined these processes in the dulotic ant Temnothorax americanus and its congeneric host Temnothorax longispinosus using population genomics, genome-wide association analyses, and transcriptomics. Host populations showed very weak and parasites stronger population structure, enabling geographic mosaic dynamics. Genomic responses to parasite prevalence were divergent: Hosts showed signatures of selection on immune genes, whereas regulatory genes associated with raiding were under selection in parasites. Both species displayed convergent signatures of climate adaptation, including loci related to desiccation resistance, stress response, and parasite prevalence, with signals in communication and recognition genes involved in hydrocarbon biosynthesis, chemosensory perception, circadian rhythms, and venom production. Transcriptome analyses revealed contrasting patterns, with host gene expression linked to parasite prevalence and parasite expression more strongly shaped by climate. Together, our results reveal a genomic mosaic of coadaptation, in which population structure, asymmetric selection, and ecological variation interact to generate divergent yet interconnected evolutionary trajectories. Our findings highlight communication and recognition as recurrent arenas of antagonistic coevolution, underscore climate as a pervasive selective force, and establish a framework for investigating molecular coevolution in social parasite systems.

Summary Overlap in habitat use between herbivores can result in facilitative interactions, through enhancement of forage quality, as well as competitive interactions. The latter result from either interference or indirectly from resource depletion. We investigated competitive and facilitative interactions between wild Barnacle and Brent Geese and European Brown Hares on a salt marsh in the Dutch Wadden Sea. In a multifactorial experimental design, we manipulated biomass and quality of grass swards and determined foraging preferences of the wild herbivores. We found that both Barnacle and Brent Geese select plots with plants that have a higher nitrogen content. Barnacle Geese avoid plots with high plant biomass. Hares prefer the combination of high biomass with high plant quality, when geese are absent. However, in the natural situation with geese present, hares select high biomass swards. Grazing increases the quality of the vegetation within one season. Geese mainly select plots that have been previously grazed by either geese or hares within the same season. We conclude that indirect competition through forage depletion by large numbers of geese in spring plays a significant role determining the foraging choices of hares, while Barnacle Geese profit from grazing facilitation by other small herbivores which prevents the maturation of forage tissues.

Nonmycorrhizal cluster root-forming species enhance the phosphorus (P) acquisition of mycorrhizal neighbours in P-impoverished megadiverse systems. However, whether mycorrhizal plants facilitate the defence of nonmycorrhizal plants against soil-borne pathogens, in return and via their symbiosis, remains unknown. We characterised growth and defence-related compounds in Banksia menziesii (nonmycorrhizal) and Eucalyptus todtiana (ectomycorrhizal, ECM) seedlings grown either in monoculture or mixture in a multifactorial glasshouse experiment involving ECM fungi and native oomycete pathogens. Roots of B. menziesii had higher levels of phytohormones (salicylic and jasmonic acids, jasmonoyl-isoleucine and 12-oxo-phytodienoic acid) than E. todtiana which further activated a salicylic acid-mediated defence response in roots of B. menziesii, but only in the presence of ECM fungi. We also found that B. menziesii induced a shift in the defence strategy of E. todtiana, from defence-related secondary metabolites (phenolic and flavonoid) towards induced phytohormone response pathways. We conclude that ECM fungi play a vital role in the interactions between mycorrhizal and nonmycorrhizal plants in a severely P-impoverished environment, by introducing a competitive component within the facilitation interaction between the two plant species with contrasting nutrient-acquisition strategies. This study sheds light on the interplay between beneficial and detrimental soil microbes that shape plant-plant interaction in severely nutrient-impoverished ecosystems.

<p>Competitive and facilitative interactions play an important role in determining plant community structure and development. Historically, competitive interactions have been considered to be more prevalent in nature. However, in the past few decades strong facilitative interactions have been identified as being more important than competition in certain environments. Recent evidence has also suggested that interactions occurring in the above and below ground environments may be unevenly contributing to the net interaction effects between a target plant and nurses species. This study partitions the above and below ground interactions and determines their strength and directions in order to help better understand their relative importance to plant community dynamics. In Chapter 2 I develop species specific allometric models which aim to accurately estimate the total above- and below- ground biomass of individual D. dacrydioides and P. totara juveniles using measurements which are easily and non-destructively obtained in the field. The best model for each species is then used to construct total above and below ground biomass estimates for use in Chapter 3. Eight models using stem height, diameter, and volume either alone or in combination are examined for their predictive power and tested for their goodness of fit. Models using diameter alone are found to be less powerful in predicting total tree biomass, while models containing height either alone or in combination with diameter are more powerful. The absolute best model for predicting D. dacrydioides total biomass was BTOTAL = 0.0099(Height²)⁰˙⁸⁷⁴⁹, whereas the absolute best model for P. totara was BTOTAL = 0.2635((Height*Diameter)²)⁰˙⁵⁶⁹⁵. In Chapter 3 I use the Relative Interaction Index (RII) to determine the strength and direction of the net interactions affecting D. dacrydioides and P. totara juveniles. To partition the above ground interactions, I examined the effects of a conspecific or interspecific neighbour. I found that my two study species D. dacrydioides and P. totara showed different responses to the treatments that they received. D. dacrydioides showed net facilitation and gained biomass when it had access to the mycorrhizal network and a neighbour. Whereas, P. totara showed net neutral interactions and did not gain biomass. P. totara also showed net competition when it did not have access to the mycorrhizal network and was grown next to neighbours. The role of above ground interactions was found to be less important than below ground interactions, overall. In general, these results mean that D. dacrydioides juveniles should be expected to have higher growth, reproductive, and survival rates when grown next to nurse species in comparison to P. totara. Chapter 4 details the significance of this study for the restoration of Wairio wetland, and wetlands in general. Given the result in chapter 3 and the current restoration method at Wairio wetland, this study suggests that it may be worth exploring the benefit of planting new P. totara juveniles farther away from older woody species in order to avoid root competition.</p>

Summary A long‐standing hypothesis in ecology and evolutionary biology is that closely related species are more ecologically similar to each other and therefore compete more strongly than distant relatives do. A recent hypothesis posits that evolutionary relatedness may also explain the prevalence of mutualisms, with facilitative interactions being more common among distantly related species. Despite the importance of these hypotheses for understanding the structure and function of ecological communities, experimental tests to determine how evolutionary relatedness influences competition and facilitation are still somewhat rare. Here, we report results of a laboratory experiment in which we assessed how competitive and facilitative interactions among eight species of freshwater green algae are influenced by their relatedness. We measured the prevalence of competition and facilitation among 28 pairs of freshwater green algal species that were chosen to span a large gradient of phylogenetic distances. For each species, we first measured its invasion success when introduced into a steady‐state population of another resident species. Then, we compared its growth rate when grown alone in monoculture to its growth rate when introduced as an invader. The change in the species' population growth rate as an invader (sensitivity) is used as a measure of the strength of its interaction with the resident species. A reduced growth rate in the presence of another species indicates competition, whereas an increased growth rate indicates facilitation. Although competition between species was more frequent (75% of interactions), facilitation was common (the other 25% of interactions). We found no significant relationship between the phylogenetic distance separating two interacting species and the success of invasion, nor the prevalence or strength of either competition or facilitation. Interspecific interactions depended more on the identity of the species, with certain taxa consistently acting as good or bad competitors/facilitators. These species were not predictable a priori from their positions on a phylogeny. Synthesis. The phylogenetic relatedness of the green algae species used here did not predict the prevalence of competitive and facilitative interactions, rejecting the hypothesis that close relatives compete strongly and contesting recent evidence that facilitation is likely to occur between distant relatives.

Author index

Several lines of evidence support the hypothesis that local populations of red crossbills (Loxia curvirostra complex) enter into a predator-prey arms race with lodgepole pine (Pinus contorta latifolia) in the absence of competing pine squirrels (Tamiasciurus hudsonicus). Nevertheless, the alternative hypotheses that neutral evolution or factors other than squirrels have caused crossbill population differentiation have not been thoroughly tested. We compared crossbill and pine cone morphology between island populations where squirrels are absent or present, and mainland sites where squirrels are present, in order to distinguish among these hypotheses. All comparisons supported an effect of squirrel absence, not island status, on crossbill and cone morphology. Hence our results provide further evidence that strong localized coevolutionary interactions in a geographic mosaic have driven adaptive population differentiation. In addition, vocal differentiation of crossbills was related to the absence of squirrels, but not to island status. As morphological and vocal differentiation is correlated with reproductive isolation in crossbills, the geographic mosaic of coevolution also seems to promote ecological speciation.

Livestock overgrazing causes environmental degradation, species invasion, biodiversity loss, and productivity decline, with profound consequences for ecological sustainability and human livelihoods. Habitat protection can mitigate such impacts, but we know little about how the long‐term recovery of plant communities from livestock overgrazing depends on the presence of encroaching shrubs. Here, we explored how shrub encroachment mediates the effects of habitat protection (i.e., livestock exclusion and creation of UNESCO protected areas) on biodiversity recovery and ecosystem functioning (i.e., biomass productivity). We leveraged a long‐term (15–25 years) experiment of livestock exclusion and complemented it with the removal of an encroaching shrub species in pasture areas and protected areas. We reveal that habitat protection has positive effects on patterns of recovery. Yet, the effects of habitat protection are mediated by shrub encroachment. Encroaching shrubs have net positive effects on plant diversity in pasture areas but inhibit biodiversity recovery in protected areas. The combination of habitat protection and the removal of encroaching shrubs best enhances the recovery of plant diversity and biomass productivity. A potential underlying mechanism is the shift in plant interactions from facilitation for recruitment and associated resistance to competition for water. Understanding species interactions is key to guiding conservation and restoration actions which can turn degraded ecosystems back into functional, species‐rich communities.

While most studies yield positive relationships between biodiversity (B) and ecosystem functioning (EF), awareness is growing that BEF relationships can vary with ecological context. The awareness has led to increased efforts to understand how contemporary environmental context modifies BEF relationships, but the role of historical context, and the mechanisms by which it may influence biodiversity effects, remains poorly understood. We examined how historical context alters plant diversity–community productivity relationships via plant species interactions in alpine grassland. We also tested how historical context modifies interactions between plants and arbuscular mycorrhizal (AM) fungi, which can potentially mediate the above processes. We studied biodiversity effects on plant community productivity at two grassland sites with different histories related to grazing intensity—heavy versus light livestock grazing—but similar current management. We assembled experimental communities of identical species composition with plants from each of the two sites in disturbed soil from a contemporary heavily grazed grassland, ranging in species richness from one to two, three and six species. Moreover, we carried out a mycorrhizal hyphae‐exclusion experiment to test how plant interactions with AM fungi influence plant responses to historical context. We detected a significantly positive diversity–productivity relationship that was driven by complementarity effects in communities composed of plants from the site without heavy‐grazing history, but no such relationship in plant communities composed of plants from the site with heavy‐grazing history. Plants from the site with heavy‐grazing history had increased competitive ability and increased yields in low‐diversity communities but disrupted complementarity effects in high‐diversity communities. Moreover, plants of one species from the site with heavy‐grazing history benefitted more from AM fungal communities than did plants from the site without such history. Synthesis. Using the same experimental design and species, communities assembled by plants from two sites with different historical contexts showed different plant diversity–community productivity relationships. Our results suggest that historical context can alter plant diversity–community productivity relationships via plant species interactions and potentially plant–soil interactions. Therefore, considering historical contexts of ecological communities is of importance for advancing our understanding of long‐term impacts of anthropogenic disturbance on ecosystem functioning.

Oceanic islands have high biodiversity due to high rates of endemicity, which is now severely threatened by global change, including biological invasions. Invasive plants are predicted to displace native plants via vigorous resource use associated with fast growth rates and population expansion. The corresponding dynamics associated with invasive plant litter offer important insights to bridge live foliage traits associated with competition with invasive plant effects on ecosystem function via litter decomposition. Evidence has accumulated to support the prediction that invasive species produce higher quality litter than native species, which decomposes more rapidly, in turn providing positive feedback that facilitates their expansion. However, litter quality can vary among and within species across climate gradients, which is likely to contribute to spatial variation in native-invasive plant interactions. In this study, we synthesize a large body of litter trait data using systematic review methods and quantitative analyses, to investigate litter trait differences between native island plants and non-native plants established in natural habitats across steep elevation (7.5 – 2660 m) and mean annual rainfall (272 – 6362 mm) gradients of the Hawaiian Islands. We found that litter traits are highly variable in both native and invasive species, with considerable overlap in multivariate trait space. Intraspecific and interspecific differences were the main sources of litter trait variation, which explained 40% and 41% of the total variance, respectively. Nonetheless, as predicted, invasive plants had litter that tended to be of higher nutritional quality and lower toughness than native plants, although this difference explained only 8% of the total variance across all traits. Interestingly, litter traits varied significantly with respect to temperature and rainfall, and the patterns differed between native and invasive plants. These results corroborate previous studies on live foliage traits that climate mediates invasive-native plant interactions across the heterogeneous environment of Hawaii. These patterns emphasize the importance of considering litter as part of the functional syndrome of plants and for a better understanding of how invasive plants may alter their novel ecosystems.

A current challenge in evolutionary ecology is to assess how the spatial structure of interacting species shapes coevolution. Previous work on the geographic mosaic of coevolution has shown that coevolution depends on the spatial structure, the strength of selection, and gene flow across populations. We used spatial subgraphs and coevolutionary models to evaluate how spatial structure and the location of coevolutionary hotspots (sites in which reciprocal selection occurs) and coldspots (sites in which unidirectional selection occurs) contribute to the dynamics of coevolution and the maintenance of polymorphisms. Specifically, we developed a new approach based on the Laplacian matrices of spatial subgraphs to explore the tendency of interacting species to evolve toward stable polymorphisms. Despite the complex interplay between gene flow and the strength of reciprocal selection, simple rules drive coevolution in small groups of spatially structured interacting populations. Hotspot location and the spatial organization of coldspots are crucial for understanding patterns in the maintenance of polymorphisms. Moreover, the degree of spatial variation in the outcomes of the coevolutionary process can be predicted from the network pattern of gene flow among sites. Our work provides us with novel tools that can be used in the field or the laboratory to predict the effects of spatial structure on coevolutionary trajectories.

Coevolutionary Biology: Sex and the Geographic Mosaic of Coevolution

Competitive and facilitative interactions within and between two species of coastal dune perennials

/ Prairie dogs (Cynomys spp.) have been labeled as keystone species because of their influence on biological diversity and ecosystem function. However, the validity of several assumptions used to support keystone status is questionable. We review the strength of the evidence and the magnitude of the prairie dog's effects on ecosystem structure and function. We use this review to reevaluate the keystone role for prairie dogs. Our goal is to encourage sound management of the prairie dog ecosystem by improving the ecological foundation of their keystone status. Our review confirms that prairie dogs affect a number of ecosystem-level functions but that their influence on prairie vertebrates may be less than previously suggested. Species richness and abundance patterns were variable among plants, mammals, and birds and were not consistently higher on prairie dog colonies compared to uncolonized areas. In addition, only nine of the 208 species listed in the literature as observed on or near prairie dogs colonies had quantitative evidence of dependence on prairie dogs. Abundance data indicated opportunistic use of colonies for an additional 20 species. A total of 117 species may have some relationship with prairie dogs, but we lacked sufficient data to evaluate the strength of this relationship. The remaining 62 species may be accidental or alien to the system. Despite our conclusion that some prairie dog functions may be smaller than previously assumed, collectively these functions are quite large compared to other herbivores in the system. We suggest that prairie dogs also provide some unique functions not duplicated by any other species and that continued decline of prairie dogs may lead to a substantial erosion of biological diversity and landscape heterogeneity across prairie and shrub-steppe landscapes. Thus, we concur that keystone status for prairie dogs is appropriate and may aid conservation efforts that help protect species dependent on prairie dogs and support other important ecosystem functions.KEY WORDS: Prairie dogs; Cynomys spp.; Keystone species; Ecosystem functions; Biological diversityhttp://link.springer-ny.com/link/service/journals/00267/bibs/24n2p177.html