Mutualistic interactions, where species reciprocally benefit from each other, are crucial for ecosystem stability and biodiversity. These interactions often involve species that experience different fitness effects for the traded resources or services. Because mutualisms rely on positive feedback between partners, such asymmetries can strongly influence evolutionary outcomes. Differences in fitness effects create divergent selective pressures, shaping trait evolution and determining the persistence of mutualisms. The strength of these effects can also vary depending on the availability of traded resources from other sources. Despite their importance, the evolutionary role of fitness asymmetries in mutualism has received little attention, beyond recognizing that some species may be more dependent on their partners than others. This study investigates how asymmetry in the fitness effects of a traded resource influences the persistence and phenotypic trait evolution of species in multi-mutualist guilds. To test this, we constructed synthetic multi-mutualist communities by combining, reproductively isolated and genetically modified strains of Saccharomyces cerevisiae that engage in a nutritional mutualism by trading adenine and lysine. One guild of four strains cannot produce lysine but overproduces adenine while the other guild cannot produce adenine but overproduces lysine. Lysine overproducers survive periods of low adenine better than adenine overproducers survive low lysine. Over a four-week evolution experiment we observed that strain persistence was strongly influenced by the availability of external resources. Communities in media containing traded resources supported the survival of all strains, whereas obligate conditions led to a significant extinction, especially for adenine overproducers. We observed distinct evolutionary trajectories of traits under obligate versus supplemented conditions. Phenotypic assays revealed that costs and benefits evolved differently depending on the essentiality of the traded resource and nutrient supplementation. These results demonstrate that asymmetries in the fitness effects of traded resources can influence evolutionary outcomes, species persistence, and community stability in multi-mutualist communities.

Coevolution is a ubiquitous driver of diversification in both mutualistic and antagonistic interactions between species. In mutualisms, coevolution can result in trait complementarity between partners that facilitates their persistence. Despite its importance, most of what we know about coevolution in mutualism comes from obligate interactions, whereas we know comparatively little about facultative interactions, arguably the most common type of mutualism. To evaluate coevolutionary dynamics in facultative mutualism and test how it compares with obligate mutualisms, we used a synthetic yeast mutualism where the partners exchange essential nutrient resources. We manipulated mutualism dependency by controlling the availability of mutualistic resources in the environment and measured coevolution via time-shift assays and tracking the evolution of mutualistic traits over time. In addition, we genotyped the evolved and ancestral mutualists to test for differences in the strength of coevolutionary selection between facultative and obligate mutualisms. We found evidence of coevolution in both facultative and obligate mutualisms, but coevolution was weaker and slower in facultative mutualisms. We also found evidence for evolution of trait complementarity in obligate mutualisms but not in facultative mutualisms. Furthermore, obligate mutualists had more SNPs under positive selection than facultative mutualists. Together, these results provide strong evidence that mutualism dependency impacts both the strength of coevolution and the rate of trait evolution.

Mutualisms are interactions among species in which the participants receive a fitness benefit. Almost all organisms are engaged in at least one mutualistic interaction and mutualisms forms the basis of many, if not all, communities and ecosystems. This article provides an overview of how these important interactions originate, remain stable, and are influenced by the presence of other species.

Although we have a good understanding of how phenotypic plasticity evolves in response to abiotic environments, we know comparatively less about responses to biotic interactions. We experimentally tested how competition and mutualism affected trait and plasticity evolution of pairwise communities of genetically modified brewer’s yeast. We quantified evolutionary changes in growth rate, resource use efficiency (RUE), and their plasticity in strains evolving alone, with a competitor, and with a mutualist. Compared to their ancestors, strains evolving alone had lower RUE and RUE plasticity. There was also an evolutionary tradeoff between changes in growth rate and RUE in strains evolving alone, suggesting selection for increased growth rate at the cost of efficiency. Strains evolving with a competitive partner had higher growth rates, slightly lower RUE, and a stronger tradeoff between growth rate and efficiency. In contrast, mutualism had opposite effects on trait evolution. Strains evolving with a mutualist had slightly lower growth rates, higher RUE, and a weak evolutionary tradeoff between growth rate and RUE. Despite their different effects on trait evolution, competition and mutualism had little effect on plasticity evolution for either trait, suggesting that abiotic factors could be more important than biotic factors in generating selection for plasticity.

Polyploid organisms are common and can be found across the tree of life. A key question is to understand how and why these polyploid lineages become established and persist in populations, particularly since they are predicted to have a low probability of success. While the collection of papers in this special issue addresses broad questions on the evolutionary ecology of polyploids, ultimately, these studies also highlight the myriad ways that we are examining what drives the success of polyploid lineages. In this paper we consider where we've been and the challenges that we face, and then propose several directions that will allow us to continue to propel the field towards our ultimate goal of understanding the rules that govern the establishment and persistence of polyploid populations. We conclude that developing this rule set will require a combination of model systems for which we have detailed knowledge of the phylogenetic and population genetic history, expanding our perspective beyond plants to include greater taxonomic breadth, and conducting studies in ecologically relevant settings. Additionally, we argue that future research on the evolutionary ecology of polyploidy should focus on integrating theory and empirical research, providing mechanistic linkages between the effects of whole genome duplication and population demography, and build a predictive framework to understand how anthropogenic change will impact polyploid organisms.

A long-standing problem in the study of mutualism is to understand the effects of non-mutualistic community members that exploit the benefits of mutualism without offering commodities in exchange (i.e., ‘exploiters’). Mutualisms are continually challenged by exploiters and their persistence may depend on the costliness of exploitation or on adaptations that allow mutualists to avoid the negative effects of exploiters. Coevolution could lead to changes in mutualists and exploiters that allow mutualisms to persist. Although coevolution is considered essential for mutualism persistence and resistance to disturbance, we have yet to obtain direct experimental evidence of the role of coevolution in resistance to exploitation. Additionally, resistance to exploitation via coevolutionary processes might vary with the degree of dependency between mutualistic partners, as facultative mutualisms are thought to be under weaker coevolutionary selection than obligate mutualisms. Here, we conducted an experimental evolution study using a synthetic yeast mutualism to test how coevolution in facultative and obligate mutualisms affects their resistance to exploitation. We found that naïve facultative mutualisms were more likely to breakdown under exploitation than naïve obligate mutualisms. After 15 weeks of coevolution, both facultative and obligate evolved mutualists were more likely to survive exploitation than naïve mutualists when we reassembled mutualist communities. Additionally, coevolved exploiters were more likely to survive with mutualists, whereas naïve exploiters frequently went extinct. These results suggest that coevolution between mutualists and exploiters can lead to mutualism persistence, potentially explaining why exploitation is ubiquitous but rarely associated with mutualism breakdown.

Host plant shifts are central to diversification in insect herbivores. Many mechanisms can cause host shifts in insects, but one relatively unexplored mechanism is whole‐genome duplication (WGD) in the host plant. WGD, or polyploidy, is common in plants and causes spontaneous changes in physiology, morphology, and palatability that could impact the ability of herbivores to feed and develop on newly formed polyploids (neopolyploids). Here the authors tested if WGD affected the preference and performance of the specialist aphid, Acyrthosiphon pisum (pea aphids). Pea aphids seasonally form specialised lineages or ‘host forms’ on many host plant species including alfalfa and red clover. Aphid host forms on alfalfa and red clover naturally exist on different cytotypes of their respective hosts, with red clover aphids feeding on diploid clover and alfalfa aphids feeding on tetraploid alfalfa. Therefore, the authors predicted that these host forms would have a higher preference for and performance on their respective natal host cytotype. Neither host form exhibited a preference for a particular cytotype, but there were modest changes in aphid performance based on host cytotype. Specifically, aphids specialised to red clover had higher fecundity on diploid red clover than on neotetraploid red clover. Together, these results showed that both host forms were able to recognise and accept different cytotypes of the two host species, but only one host form experienced trade‐offs in performance when feeding on neotetraploids. These results suggest that WGD may act as a mechanism of host expansion in pea aphids as plants speciate via WGD.

Functional traits fall along a continuum from resource conservative to acquisitive and are powerful predictors of the ecological settings necessary for a species to persist and establish. As a consequence, a major problem that functional trait analysis could address is understanding the ecological contexts necessary for the persistence of polyploid plants, because early generation polyploids, or "neopolyploids," are at a high extinction risk. Because neopolyploidy could increase nutrient limitation, growth strategies should shift to accommodate the increased need for resources, but this prediction is untested. To address this gap, we compared the functional trait responses of diploids, synthetic neotetraploids, and naturally occurring tetraploids of Heuchera cylindrica, an herbaceous perennial plant, to nutrient manipulations in a greenhouse experiment. We found strong support for the hypothesis that neotetraploidy increases nutrient requirements, as evidenced by reduced productivity and increased tissue concentrations of nitrogen and phosphorus in neotetraploids. We also found that the repeated formation of independent origins of neotetraploidy led to differing responses to nutrient supply, but neotetraploidy generally shifted functional traits to be more resource acquisitive and inefficient. Taken together, our results suggest that shifts in functional trait responses may constrain the ability of neopolyploids to establish in nutrient-poor habitats.

Species interactions shape the evolution of traits, life histories and the pattern of speciation. What is less clear is whether certain types of species interaction are more or less likely to lead to phenotypic divergence among species. We used the brood pollination mutualism between yuccas and yucca moths to test how mutualistic (pollination) and antagonistic (oviposition) traits differ in the propensity to increase phenotypic divergence among pollinator moths. We measured traits of the tentacular mouthparts, structures used by females to actively pollinate flowers, as well as ovipositor traits to examine differences in the rate of evolution of these two suites of traits among pollinator species. Morphological analyses revealed two distinct groups of moths based on ovipositor morphology, but no such groupings were identified for tentacle morphology, even for moths that pollinated distantly related yuccas. In addition, ovipositor traits evolved at significantly faster rates than tentacular traits. These results support theoretical work suggesting that antagonism is more likely than mutualism to lead to phenotypic divergence.

Switching to a new host plant is a driving force for divergence and speciation in herbivorous insects. This process of incorporating a novel host plant into the diet may require a number of adaptations in the insect herbivores that allow them to consume host plant tissue that may contain toxic secondary chemicals. As a result, herbivorous insects are predicted to have evolved efficient ways to detoxify major plant defences and increase fitness by either relying on their own genomes or by recruiting other organisms such as microbial gut symbionts. In the present study we used parallel metatranscriptomic analyses of Altica flea beetles and their gut symbionts to explore the contributions of beetle detoxification mechanisms versus detoxification by their gut consortium. We compared the gut meta-transcriptomes of two sympatric Altica species that feed exclusively on different host plant species as well as their F1 hybrids that were fed one of the two host plant species. These comparisons revealed that gene expression patterns of Altica are dependent on both beetle species identity and diet. The community structure of gut symbionts was also dependent on the identity of the beetle species, and the gene expression patterns of the gut symbionts were significantly correlated with beetle species and plant diet. Some of the enriched genes identified in the beetles and gut symbionts are involved in the degradation of secondary metabolites produced by plants, suggesting that Altica flea beetles may use their gut microbiota to help them feed on and adapt to their host plants.

Species interactions shape the evolution of traits, life histories and the pattern of speciation. What is less clear is whether certain types of species interaction are more or less likely to lead to phenotypic divergence among species. We used the brood pollination mutualism between yuccas and yucca moths to test how mutualistic (pollination) and antagonistic (oviposition) traits differ in the propensity to increase phenotypic divergence among pollinator moths. We measured traits of the tentacular mouthparts, structures used by females to actively pollinate flowers, as well as ovipositor traits to examine differences in the rate of evolution of these two suites of traits among pollinator species. Morphological analyses revealed two distinct groups of moths based on ovipositor morphology, but no such groupings were identified for tentacle morphology, even for moths that pollinated distantly related yuccas. In addition, ovipositor traits evolved at significantly faster rates than tentacular traits. These results support theoretical work suggesting that antagonism is more likely than mutualism to lead to phenotypic divergence.

The obligate pollination mutualism between Yucca and yucca moths is a classical example of coevolution. Oviposition and active pollination by female yucca moths occur at night when Yucca flowers are open and strongly scented. Thus, floral volatiles have been suggested as key sensory signals attracting yucca moths to their host plants, but no bioactive compounds have yet been identified. In this study, we showed that both sexes of the pollinator moth Tegeticula yuccasella are attracted to the floral scent of the host Yucca filamentosa. Chemical analysis of the floral headspace from six Yucca species in sections Chaenocarpa and Sarcocarpa revealed a set of novel tetranorsesquiterpenoids putatively derived from (E)-4,8-dimethyl-1,3,7-nonatriene. Their structure elucidation was accomplished by NMR analysis of the crude floral scent sample of Yucca treculeana along with GC/MS analysis and confirmed by total synthesis. Since all these volatiles are included in the floral scent of Y. filamentosa, which has been an important model species for understanding the pollination mutualism, we name these compounds filamentolide, filamentol, filamental, and filamentone. Several of these compounds elicited antennal responses in pollinating (Tegeticula) and non-pollinating (Prodoxus) moth species upon stimulation in electrophysiological recordings. In addition, synthetic (Z)-filamentolide attracted significant numbers of both sexes of two associated Prodoxus species in a field trapping experiment. Highly specialized insect-plant interactions, such as obligate pollination mutualisms, are predicted to be maintained through "private channels" dictated by specific compounds. The identification of novel bioactive tetranorsesquiterpenoids is a first step in testing such a hypothesis in the Yucca-yucca moth interaction.

Insect mutualisms are essential for reproduction of many plants, protection of plants and other insects, and provisioning of nutrients for insects. Disruption of these mutualisms by global change can have important implications for ecosystem processes. Here, we assess the general effects of global change on insect mutualisms, including the possible impacts on mutualistic networks. We find that the effects of global change on mutualisms are extremely variable, making broad patterns difficult to detect. We require studies focusing on changes in cost-benefit ratios, effects of partner dependency, and degree of specialization to further understand how global change will influence insect mutualism dynamics. We propose that rapid coevolution is one avenue by which mutualists can ameliorate the effects of global change.

The mango seed weevil Sternochetus mangiferae (Fabricius) is distributed across the major mango‐producing areas of the world and causes significant economic losses of mango fruit. Despite its importance as a crop pest, we have only limited information on the population genetics of the mango seed weevil. Here, we examined the genetic diversity of this important pest using specimens intercepted by Beijing Customs District P. R. in China from 41 countries and regions. We used segments of the mitochondrial gene cytochrome c oxidase subunit I and the nuclear gene elongation factor 1‐alpha to examine population genetic structure in this species. Our results showed that genetic diversity is low in S. mangiferae , with a mean genetic distance of 0.095–0.14%. Other population genetic parameters also indicated a low level of genetic diversity among samples from a large geographic range. Analysis of molecular variance revealed little population genetic structure, and mismatch distribution analyses provided evidence of a population expansion, although other demographic metrics of population expansion were nonsignificant. We suggest that the observed low level of genetic diversity and population genetic structure in S. mangiferae supports the hypothesis that the population genetics of this species has been impacted by anthropogenic transportation of mangoes and weevils.

Understanding how mutualisms persist over time requires investigations of how mutualist species coevolve and adapt to the interaction. In particular, the key factors in the evolution of mutualisms are the costs and benefits mutualists experience during the interaction. Here, we used a yeast nutritional mutualism to test how mutualists coevolve and adapt in an obligate mutualism. We allowed two yeast mutualists to evolve together for 15 weeks (about 150 generations), and then we tested if the mutualists had coevolved using time-shift assays. We also examined two mutualistic traits associated with the costs and benefits: resource use efficiency and commodity production. We found that the mutualists quickly coevolved. Furthermore, the changes in benefits and costs were nonlinear and varied with evolutionary changes occurring in the mutualist partner. One mutualist initially evolved to reduce mutualistic commodity production and increase efficiency in mutualistic resource use; however, this negatively affected its mutualist partner that evolved reduced commodity production and resource use efficiency. As a result, the former increased commodity production, resulting in an increase in benefits for its partner. The quick, nonlinear, and asynchronous evolution of yeast mutualists closely resembles antagonistic coevolutionary patterns, supporting the view that mutualisms should be considered as reciprocal exploitation.

PREMISEAlthough polyploidy has been studied since the early 1900s, fundamental aspects of polyploid ecology and evolution remain unexplored. In particular, surprisingly little is known about how newly formed polyploids (neopolyploids) become demographically established. Models predict that most polyploids should go extinct within the first few generations as a result of reproductive disadvantages associated with being the minority in a primarily diploid population (i.e., the minority cytotype principle), yet polyploidy is extremely common. Therefore, a key goal in the study of polyploidy is to determine the mechanisms that promote polyploid establishment in nature. Because premating isolation is critical in order for neopolylpoids to avoid minority cytotype exclusion and thus facilitate establishment, we examined floral morphology and three common premating barriers to determine their importance in generating reproductive isolation of neopolyploids from diploids.METHODSWe induced neopolyploidy in Trifolium pratense and compared their floral traits to the diploid progenitors. In addition to shifts in floral morphology, we examined three premating barriers: isolation by self-fertilization, flowering-time asynchrony, and pollinator-mediated isolation.RESULTSWe found significant differences in the morphology of diploid and neopolyploid flowers, but these changes did not facilitate premating barriers that would generate reproductive isolation of neopolyploids from diploids. There was no difference in flowering phenology, pollinator visitation, or selfing between the cytotypes.CONCLUSIONSOur results indicate that barriers other than the ones tested in this study-such as geographic isolation, vegetative reproduction, and pistil-stigma incompatibilities-may be more important in facilitating isolation and establishment of neopolyploid T. pratense.

Mutualisms, or reciprocally beneficial interspecific interactions, constitute the foundation of many ecological communities and agricultural systems. Mutualisms come in different forms, from pairwise interactions to extremely diverse communities, and they are continually challenged with exploitation by nonmutualistic community members (exploiters). Thus, understanding how mutualisms persist remains an essential question in ecology. Theory suggests that high species richness and functional redundancy could promote mutualism persistence in complex mutualistic communities. Using a yeast system (Saccharomyces cerevisiae), we experimentally show that communities with the greatest mutualist richness and functional redundancy are nearly two times more likely to survive exploitation than are simple communities. Persistence increased because diverse communities were better able to mitigate the negative effects of competition with exploiters. Thus, large mutualistic networks may be inherently buffered from exploitation.

Premise of the StudyPolyploidy, or whole genome duplication (WGD), is common in plants despite theory suggesting that polyploid establishment is challenging and polyploids should be evolutionarily transitory. There is renewed interest in understanding the mechanisms that could facilitate polyploid establishment and explain their pervasiveness in nature. In particular, premating isolation from their diploid progenitors is suggested to be a crucial factor. To evaluate how changes in assortative mating occur, we need to understand the phenotypic effects of WGD on reproductive traits. MethodsWe used literature surveys and a meta-analysis to assess how WGD affects floral morphology, flowering phenology, and reproductive output in plants. We focused specifically on comparisons of newly generated polyploids (neopolyploids) and their parents to mitigate potential confounding effects of adaptation and drift that may be present in ancient polyploids. Key ResultsThe results indicated that across a broad representation of angiosperms, floral morphology traits increased in size, reproductive output decreased, and flowering phenology was unaffected by WGD. Additionally, we found that increased trait variation after WGD was uncommon for the phenotypic traits examined. ConclusionsOur results suggest that the phenotypic effects on traits important to premating isolation of neopolyploids are small, in general. Changes in flowering phenology, reproductive output, and phenotypic variation resulting from WGD may be less critical in facilitating premating isolation and neopolyploid establishment. However, floral traits for which size is an important component of function (e.g., pollen transfer) could be strongly influenced by WGD.

PREMISE Polyploidy is known to cause physiological changes in plants which, in turn, can affect species interactions. One major physiological change predicted in polyploid plants is a heightened demand for growth-limiting nutrients. Consequently, we expect polyploidy to cause an increased reliance on the belowground mutualists that supply these growth-limiting nutrients. An important first step in investigating how polyploidy affects nutritional mutualisms in plants, then, is to characterize differences in the rate at which diploids and polyploids interact with belowground mutualists. METHODS We used Heuchera cylindrica (Saxifragaceae) to test how polyploidy influences interactions with arbuscular mycorrhizal fungi (AMF). Here we first confirmed the presence of AMF in H. cylindrica, and then we used field-collected specimens to quantify and compare the presence of AMF structures while controlling for site-specific variation. RESULTS Tetraploids had higher colonization rates as measured by total, hyphal, and nutritional-exchange structures; however, we found that diploids and tetraploids did not differ in vesicle colonization rates. CONCLUSIONS The results suggest that polyploidy may alter belowground nutritional mutualisms with plants. Because colonization by nutritional-exchange structures was higher in polyploids but vesicle colonization was not, polyploids might form stronger associations with their AMF partners. Controlled experiments are necessary to test whether this pattern is driven by the direct effect of polyploidy on AMF colonization.