Pineapple (Ananas comosus (L.) Merr.) is the most economically valuable crop possessing crassulacean acid metabolism (CAM), a photosynthetic carbon assimilation pathway with high water use efficiency, and the second most important tropical fruit after banana in terms of international trade. We sequenced the genomes of pineapple varieties ‘F153’ and ‘MD2’, and a wild pineapple relative A. bracteatus accession CB5. The pineapple genome has one fewer ancient whole genome duplications than sequenced grass genomes and, therefore, provides an important reference for elucidating gene content and structure in the last common ancestor of extant members of the grass family (Poaceae). Pineapple has a conserved karyotype with seven pre rho duplication chromosomes that are ancestral to extant grass karyotypes. The pineapple lineage has transitioned from C3 photosynthesis to CAM with CAM-related genes exhibiting a diel expression pattern in photosynthetic tissues using beta-carbonic anhydrase (βCA) for initial capture of CO2. Promoter regions of all three βCA genes contain a CCA1 binding site that can bind circadian core oscillators. CAM pathway genes were enriched with cis-regulatory elements including the morning (CCACAC) and evening (AAAATATC) elements associated with regulation of circadian-clock genes, providing the first link between CAM and the circadian clock regulation. Gene-interaction network analysis revealed both activation and repression of regulatory elements that control key enzymes in CAM photosynthesis, indicating that CAM evolved by reconfiguration of pathways preexisting in C3 plants. Pineapple CAM photosynthesis is the result of regulatory neofunctionalization of preexisting gene copies and not acquisition of neofunctionalized genes via whole genome or tandem gene duplication.
Contents 38I.38II.Approaches for reconstructing refugia: strengths, limitations and recent advances39III.46IV.47V.48VI.4949References49 Summary Climate refugia, locations where taxa survive periods of regionally adverse climate, are thought to be critical for maintaining biodiversity through the glacial–interglacial climate changes of the Quaternary. A critical research need is to better integrate and reconcile the three major lines of evidence used to infer the existence of past refugia – fossil records, species distribution models and phylogeographic surveys – in order to characterize the complex spatiotemporal trajectories of species and populations in and out of refugia. Here we review the complementary strengths, limitations and new advances for these three approaches. We provide case studies to illustrate their combined application, and point the way towards new opportunities for synthesizing these disparate lines of evidence. Case studies with European beech, Qinghai spruce and Douglas‐fir illustrate how the combination of these three approaches successfully resolves complex species histories not attainable from any one approach. Promising new statistical techniques can capitalize on the strengths of each method and provide a robust quantitative reconstruction of species history. Studying past refugia can help identify contemporary refugia and clarify their conservation significance, in particular by elucidating the fine‐scale processes and the particular geographic locations that buffer species against rapidly changing climate.
Several mechanisms are expected to rapidly rid mutualisms of genetic variation in partner quality. Variation for mutualist quality, however, appears to be widespread. We used a model legume-rhizobium mutualism to test for evidence that context-dependent selection may maintain variation in partner quality. In a greenhouse experiment using 10 natural populations of Medicago truncatula and two strains of Sinorhizobium medicae, we detected significant genotype x genotype (G x G) interactions for plant fitness, indicating that the most beneficial rhizobium strain depends on the host genotype. In a second experiment using a subset of the plant populations used in the first experiment, we detected significant G x G interactions for both plant and rhizobium fitness. Moreover, the plant population with which rhizobium strains gained the greatest benefit depended on the nitrogen environment. Finally, we found that in a high nitrogen environment, all plant populations had lower fitness when inoculated with a 1:1 mixture of strains than with the worse single strain alone, suggesting that nitrogen shifts the exchange of benefits in favour of rhizobia. Our data suggest that genotype, nitrogen and biotic dependency might contribute to the maintenance of genetic variation in mutualist quality when coupled with spatial or temporal heterogeneity in the environment.
Studying how the fitness benefits of mutualism differ among a wide range of partner genotypes, and at multiple spatial scales, can shed light on the processes that maintain mutualism and structure coevolutionary interactions. Using legumes and rhizobia from three natural populations, I studied the symbiotic fitness benefits for both partners in 108 plant maternal family by rhizobium strain combinations. Genotype-by-genotype (G × G) interactions among local genotypes and among partner populations determined, in part, the benefits of mutualism for both partners; for example, the fitness effects of particular rhizobium strains ranged from uncooperative to mutualistic depending on the plant family. Correlations between plant and rhizobium fitness benefits suggest a trade off, and therefore a potential conflict, between the interests of the two partners. These results suggest that legume-rhizobium mutualisms are dynamic at multiple spatial scales, and that strictly additive models of mutualism benefits may ignore dynamics potentially important to both the maintenance of genetic variation and the generation of geographic patterns in coevolutionary interactions.K E Y W O R D S : G × G, genetic correlation, genotype-genotype interaction, local adaptation, Medicago truncatula, Sinorhizobium.
Preferential rewarding of more beneficial partners may stabilize mutualisms against the invasion of less beneficial, that is cheater, genotypes. Recent evidence suggests that both partner choice and sanctioning may play roles in preventing the invasion of less-beneficial rhizobia in legume-rhizobium mutualisms. The importance of these mechanisms in natural communities, however, remains unclear. We grew 12 Medicago truncatula maternal families with a mixture of three rhizobium strains from their native range for three plant generations and estimated the symbiotic benefits (nodule number and size) conferred to each rhizobium strain. In this experiment, the majority of M. truncatula genotypes formed more nodules with more beneficial rhizobium strains, providing evidence for adaptive partner choice. We also found that three generations of symbiosis resulted in an increase in the relative frequency of rhizobium strains that were most beneficial to plants-suggesting that partner choice affects rhizobium fitness. By contrast, we found no evidence that plants differentially rewarded rhizobia postnodulation via sanctioning leading to differences in nodule size. Taken together, our data suggest that plants have evolved to recognize beneficial rhizobial signals during the early stages of symbiosis, and that signaling between plants and rhizobia may be subject to coevolutionary pressures.
Human activities have altered the global nitrogen (N) cycle, and as a result, elevated N inputs are causing profound ecological changes in diverse ecosystems. The evolutionary consequences of this global change have been largely ignored even though elevated N inputs are predicted to cause mutualism breakdown and the evolution of decreased cooperation between resource mutualists. Using a long-term (22 years) N-addition experiment, we find that elevated N inputs have altered the legume-rhizobium mutualism (where rhizobial bacteria trade N in exchange for photosynthates from legumes), causing the evolution of less-mutualistic rhizobia. Plants inoculated with rhizobium strains isolated from N-fertilized treatments produced 17-30% less biomass and had reduced chlorophyll content compared to plants inoculated with strains from unfertilized control plots. Because the legume-rhizobium mutualism is the major contributor of naturally fixed N to terrestrial ecosystems, the evolution of less-cooperative rhizobia may have important environmental consequences.
The paradox of mutualism is typically framed as the persistence of interspecific cooperation, despite the potential advantages of cheating. Thus, mutualism research has tended to focus on stabilizing mechanisms that prevent the invasion of low-quality partners.These mechanisms alone cannot explain the persistence of variation for partner quality observed in nature, leaving a large gap in our understanding of how mutualisms evolve. Studying partner quality variation is necessary for applying genetically explicit models to predict evolution in natural populations, a necessary step for understanding the origins of mutualisms as well as their ongoing dynamics. An evolutionary genetic approach, which is focused on naturally occurring mutualist variation, can potentially synthesize the currently disconnected fields of mutualism evolution and coevolutionary genetics. We outline explanations for the maintenance of genetic variation for mutualism and suggest approaches necessary to address them. K E Y W O R D S :Coevolution, cooperation, partner choice, partner fidelity feedback, public goods, quantitative genetics, screening.The evolutionary paradox of interspecific mutualisms, as typically posed, refers to the apparent disagreement between theoretical predictions that (all else being equal) selection should favor cheaters, and empirical observations of generally positive interactions and long-term cooperation between species. Theoretical and empirical studies alike, motivated by this seeming paradox, have made much progress toward understanding the selective mechanisms that favor interspecific mutualism and thus explaining the long-term persistence of mutualisms despite the potential fitness advantages of cheating (Bshary and Grutter 2002;Kiers et al. 2003;Sachs et al. 2004;Heath and Tiffin 2009;Leigh 2010;Archetti et al. 2011b;Jander et al. 2012). Here we argue, however, that we are missing a fundamental aspect of mutualism evolution that would allow faster progress toward understanding the more general question of how mutualisms evolve, in the larger context of species interactions, as opposed to simply what selects for cooperative mutualist partners. We suggest that a critical question in mutualism evolution is what maintains genetic variation for partner quality in mutualisms?Answering this question will require researchers to apply evolutionary genetic methods to the study of genetic variation in mutualisms. Viewing mutualistic interactions through the lens of the maintenance of genetic variation, a classic framework shared by all of evolutionary biology, can (1) bridge the divide between the largely disconnected fields of coevolutionary genetics and mutualism evolution; and (2) provide a more predictive understanding of how mutualisms evolve. Given the importance of these interactions to natural and managed systems, including human health, a predictive understanding of mutualism evolution is an important goal. We first define what we mean by "genetic variation in mutualism," then describe why we believe that it i...
Cheating is a focal concept in the study of mutualism, with the majority of researchers considering cheating to be both prevalent and highly damaging. However, current definitions of cheating do not reliably capture the evolutionary threat that has been a central motivation for the study of cheating. We describe the development of the cheating concept and distill a relative-fitness-based definition of cheating that encapsulates the evolutionary threat posed by cheating, i.e. that cheaters will spread and erode the benefits of mutualism. We then describe experiments required to conclude that cheating is occurring and to quantify fitness conflict more generally. Next, we discuss how our definition and methods can generate comparability and integration of theory and experiments, which are currently divided by their respective prioritisations of fitness consequences and traits. To evaluate the current empirical evidence for cheating, we review the literature on several of the best-studied mutualisms. We find that although there are numerous observations of low-quality partners, there is currently very little support from fitness data that any of these meet our criteria to be considered cheaters. Finally, we highlight future directions for research on conflict in mutualisms, including novel research avenues opened by a relative-fitness-based definition of cheating.
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