bioRxiv Science⌕ Search

bioRxiv · 10.1101/242834

Symbiont switching and alternative resource acquisition strategies drive mutualism breakdown

Abstract

Cooperative interactions among species, termed mutualisms, have played a crucial role in the evolution of life on Earth. However, despite key potential benefits to partners, there are many cases where two species cease to cooperate, and mutualisms break down. What factors drive the evolutionary breakdown of mutualism? We examined the pathways towards breakdowns of the mutualism between plants and arbuscular mycorrhizal (AM) fungi. Using a comparative approach, we identify ~25 independent cases of complete mutualism breakdown across global seed plants. We found that breakdown of cooperation was only stable when host plants either: (i) partner with other root symbionts or (ii) evolve alternative resource acquisition strategies. Our results suggest that key mutualistic services are only permanently lost if hosts evolve alternative symbioses or adaptations.\n\nSignificance StatementCooperative interactions among species - mutualisms - are major sources of evolutionary innovation. However, despite their importance, two species that formerly cooperated sometimes cease their partnership. Why do mutualisms breakdown? We asked this question in the partnership between arbuscular mycorrhizal (AM) fungi and their plant hosts, one of the most ancient mutualisms. We analyse two potential trajectories towards evolutionary breakdown of their cooperation, symbiont switching and mutualism abandonment. We find evidence that plants stop interacting with AM fungi when they switch to other microbial mutualists or when they evolve alternative strategies to extract nutrients from the environment. Our results show vital cooperative interactions can be lost - but only if successful alternatives evolve.

Source connections

Explore related subjects

Keep this discovery

Explore connections, maps & timelines

BibTeXRIS

Werner, G. D. A., Cornelissen, J. H. C., Cornwell, W. K., Soudzilovskaia, N. A., Kattge, J., West, S. A., Kiers, E. T.. 2018-01-04. Symbiont switching and alternative resource acquisition strategies drive mutualism breakdown. https://doi.org/10.1101/242834

Cite the original work for its findings. Save a collection to share your selection of sources.

KEEP EXPLORING

Related preprints

A Deep Phylogenetic Split Between Short- and Long-Wavelength-Tuned Visual Systems in Surgeonfishes (Acanthuridae)

The light environment, coupled with ecology, is widely thought to drive visual adaptation, creating species-specific visual niches. However, coral reef ecosystems experience continuous spatiotemporal variations in light conditions, and mechanisms such as phenotypic plasticity may be essential for coral reef animals to adjust to such changing sensory requirements. It remains unclear how widespread colour vision plasticity is, or the extent to which ecology and phylogeny drive plasticity in coral reef fishes. Using a comparative transcriptomic approach across 22 species, we aimed to investigate visual plasticity within a prominent coral reef fish family, surgeonfishes (Acanthuridae), in response to changes in the light environment throughout development and across seasons in adults. Surprisingly, we uncovered a deep phylogenetic split (~42 mya) in visual opsin gene expression profiles, with Nasinae expressing a shorter-shifted palette than Acanthurinae, which coincides with the divide between water-column and benthic-feeding modalities during the speciation of their last common ancestor. However, opsin gene expression showed little variation in response to seasonal or ontogenetic shifts in the light environment, nor in the broad functional feeding groups extant species from both subfamilies fall under. Thus, the invariable visual gene expression observed in present-day surgeonfishes appears to be dictated by phylogenetic inertia, despite rapid diversification into a range of ecological niches. This suggests that spectral tuning into two main modalities, short and long, reduces the need for visual plasticity, allowing larger and more mobile coral reef fishes to conduct visually guided behaviours across the entire range of light environments they encounter.

evolutionary biology↗

Efficient growth factor production stabilizes cooperation in a cellular public goods game

Eukaryotic cells secrete growth factors that facilitate the proliferation and survival of neighboring cells in a coordinated manner essential for tissue development, repair, and homeostasis. However, mutant cells that fail to produce these factors may exploit the benefits provided by neighboring producers, thereby gaining a proliferative advantage that could lead to the extinction of the producer clone. Evolutionary theory predicts that preventing this "tragedy of the commons" requires a fixed spatial structure or other mechanisms that enable cells to interact preferentially with copies of themselves. Contrary to this expectation, we found that, in competition experiments, cells producing the diffusible growth factor interleukin-3 (IL3) resist invasion by non-producing mutant cells even in well-mixed populations, and that non-producers are driven to extinction instead. Using evolutionary game theory, we show that this outcome arises when the cost-to-benefit ratio of growth factor production falls below a critical threshold. We derive this tipping point analytically across the full parameter space of benefit function shape and group size and confirm that IL3 production in our experimental system satisfies this condition with a production cost less than 0.1% of the benefit conferred. These results demonstrate that efficient public good production alone can resolve the tragedy of the commons in populations of cells, and potentially in other biological systems.

evolutionary biology↗

Repeated Transitions in Migratory Behavior Across a Songbird Radiation Are Not Driven by Selection on Shared Variation in Candidate Genes

Understanding the mechanisms facilitating the repeated evolution of traits is a core question in evolutionary biology. While repeated evolution has been observed across many systems, behavioral phenotypes have been less well studied than morphological traits. Migration is a behavioral adaptation to seasonality that has evolved independently in many animals, and repeated gains and losses of migratory behavior have been especially prevalent throughout the diversification of birds. While migratory traits are heritable in many taxa and candidate genes underlying intraspecific variation in migratory behavior have been identified, whether similar genetic changes are responsible for the repeated evolution of migration remains poorly understood. We used a phylogenomic approach to investigate the relationship between variation in candidate genes and migratory propensity across nearly all species in the parulid warbler radiation (n = 101), a group of songbirds in which migratory behavior has been lost and gained multiple times. Comparisons of candidate gene tree topologies to the parulid warbler species tree revealed cases of discordance, though these were explained by differences in the number of phylogenetically informative sites among genes rather than by elevated genetic similarity among species sharing migratory strategies. Testing models of coding sequence evolution identified sites with elevated dN/dS in five candidate genes, suggestive of positive selection; however, variation at these sites showed no clear association with migratory strategy, nor did we detect recurrent selection across lineages where transitions in migratory behavior most likely occurred. Together, these results contradict the hypothesis that selection on shared variation (ancestral polymorphisms or introgressed alleles) facilitated the repeated evolution of migration in this clade.

evolutionary biology↗