Towards evolutionary predictions: Current promises and challenges.

Evolution has traditionally been a historical and descriptive science, and predicting future evolutionary processes has long been considered impossible. However, evolutionary predictions are increasingly being developed and used in medicine, agriculture, biotechnology and conservation biology. Evolutionary predictions may be used for different purposes, such as to prepare for the future, to try and change the course of evolution or to determine how well we understand evolutionary processes. Similarly, the exact aspect of the evolved population that we want to predict may also differ. For example, we could try to predict which genotype will dominate, the fitness of the population or the extinction probability of a population. In addition, there are many uses of evolutionary predictions that may not always be recognized as such. The main goal of this review is to increase awareness of methods and data in different research fields by showing the breadth of situations in which evolutionary predictions are made. We describe how diverse evolutionary predictions share a common structure described by the predictive scope, time scale and precision. Then, by using examples ranging from SARS-CoV2 and influenza to CRISPR-based gene drives and sustainable product formation in biotechnology, we discuss the methods for predicting evolution, the factors that affect predictability and how predictions can be used to prevent evolution in undesirable directions or to promote beneficial evolution (i.e. evolutionary control). We hope that this review will stimulate collaboration between fields by establishing a common language for evolutionary predictions.

Mycorrhizal fungi control phosphorus value in trade symbiosis with host roots when exposed to abrupt 'crashes' and 'booms' of resource availability.

Biological market theory provides a conceptual framework to analyse trade strategies in symbiotic partnerships. A key prediction of biological market theory is that individuals can influence resource value - meaning the amount a partner is willing to pay for it - by mediating where and when it is traded. The arbuscular mycorrhizal symbiosis, characterised by roots and fungi trading phosphorus and carbon, shows many features of a biological market. However, it is unknown if or how fungi can control phosphorus value when exposed to abrupt changes in their trade environment. We mimicked an economic 'crash', manually severing part of the fungal network (Rhizophagus irregularis) to restrict resource access, and an economic 'boom' through phosphorus additions. We quantified trading strategies over a 3-wk period using a recently developed technique that allowed us to tag rock phosphate with fluorescing quantum dots of three different colours. We found that the fungus: compensated for resource loss in the 'crash' treatment by transferring phosphorus from alternative pools closer to the host root (Daucus carota); and stored the surplus nutrients in the 'boom' treatment until root demand increased. By mediating from where, when and how much phosphorus was transferred to the host, the fungus successfully controlled resource value.

Compartmentalization drives the evolution of symbiotic cooperation.

Across the tree of life, hosts have evolved mechanisms to control and mediate interactions with symbiotic partners. We suggest that the evolution of physical structures that allow hosts to spatially separate symbionts, termed compartmentalization, is a common mechanism used by hosts. Such compartmentalization allows hosts to: (i) isolate symbionts and control their reproduction; (ii) reward cooperative symbionts and punish or stop interactions with non-cooperative symbionts; and (iii) reduce direct conflict among different symbionts strains in a single host. Compartmentalization has allowed hosts to increase the benefits that they obtain from symbiotic partners across a diversity of interactions, including legumes and rhizobia, plants and fungi, squid and Vibrio, insects and nutrient provisioning bacteria, plants and insects, and the human microbiome. In cases where compartmentalization has not evolved, we ask why not. We argue that when partners interact in a competitive hierarchy, or when hosts engage in partnerships which are less costly, compartmentalization is less likely to evolve. We conclude that compartmentalization is key to understanding the evolution of symbiotic cooperation. This article is part of the theme issue 'The role of the microbiome in host evolution'.

TRY plant trait database - enhanced coverage and open access.

Plant traits-the morphological, anatomical, physiological, biochemical and phenological characteristics of plants-determine how plants respond to environmental factors, affect other trophic levels, and influence ecosystem properties and their benefits and detriments to people. Plant trait data thus represent the basis for a vast area of research spanning from evolutionary biology, community and functional ecology, to biodiversity conservation, ecosystem and landscape management, restoration, biogeography and earth system modelling. Since its foundation in 2007, the TRY database of plant traits has grown continuously. It now provides unprecedented data coverage under an open access data policy and is the main plant trait database used by the research community worldwide. Increasingly, the TRY database also supports new frontiers of trait-based plant research, including the identification of data gaps and the subsequent mobilization or measurement of new data. To support this development, in this article we evaluate the extent of the trait data compiled in TRY and analyse emerging patterns of data coverage and representativeness. Best species coverage is achieved for categorical traits-almost complete coverage for 'plant growth form'. However, most traits relevant for ecology and vegetation modelling are characterized by continuous intraspecific variation and trait-environmental relationships. These traits have to be measured on individual plants in their respective environment. Despite unprecedented data coverage, we observe a humbling lack of completeness and representativeness of these continuous traits in many aspects. We, therefore, conclude that reducing data gaps and biases in the TRY database remains a key challenge and requires a coordinated approach to data mobilization and trait measurements. This can only be achieved in collaboration with other initiatives.

Mycorrhizal Fungi Respond to Resource Inequality by Moving Phosphorus from Rich to Poor Patches across Networks.

The world's ecosystems are characterized by an unequal distribution of resources [1]. Trade partnerships between organisms of different species-mutualisms-can help individuals cope with such resource inequality [2-4]. Trade allows individuals to exchange commodities they can provide at low cost for resources that are otherwise impossible or more difficult to access [5, 6]. However, as resources become increasingly patchy in time or space, it is unknown how organisms alter their trading strategies [7, 8]. Here, we show how a symbiotic fungus mediates trade with a host root in response to different levels of resource inequality across its network. We developed a quantum-dot-tracking technique to quantify phosphorus-trading strategies of arbuscular mycorrhizal fungi simultaneously exposed to rich and poor resource patches. By following fluorescent nanoparticles of different colors across fungal networks, we determined where phosphorus was hoarded, relocated, and transferred to plant hosts. We found that increasing exposure to inequality stimulated trade. Fungi responded to high resource variation by (1) increasing the total amount of phosphorus distributed to host roots, (2) decreasing allocation to storage, and (3) differentially moving resources within the network from rich to poor patches. Using single-particle tracking and high-resolution video, we show how dynamic resource movement may help the fungus capitalize on value differences across the trade network, physically moving resources to areas of high demand to gain better returns. Such translocation strategies can help symbiotic organisms cope with exposure to resource inequality.

Match and mismatch between dietary switches and microbial partners in plant sap-feeding insects.

Some animal groups associate with the same vertically transmitted microbial symbionts over extended periods of evolutionary time, punctuated by occasional symbiont switches to different microbial taxa. Here we test the oft-repeated suggestion that symbiont switches are linked with host diet changes, focusing on hemipteran insects of the suborder Auchenorrhyncha. These insects include the only animals that feed on plant xylem sap through the life cycle, as well as taxa that feed on phloem sap and plant parenchyma cells. Ancestral state reconstruction provides strong statistical support for a xylem feeding auchenorrhynchan ancestor bearing the dual symbiosis with the primary symbiont Sulcia (Bacteroidetes) and companion symbiont 'ß-Sym' (ß-proteobacteria). We identified seven dietary transitions from xylem feeding (six to phloem feeding, one to parenchyma feeding), but no reversions to xylem feeding; five evolutionary losses of Sulcia, including replacements by yeast symbionts, exclusively in phloem/parenchyma-feeding lineages; and 14-15 losses of ß-Sym, including nine transitions to a different bacterial companion symbiont. Our analysis indicates that, although companion symbiont switching is not associated with shifts in host diet, Sulcia is probably required for xylem-feeding. Furthermore, the ancestral auchenorrhynchan bearing Sulcia and ß-Sym probably represents the sole evolutionary origin of xylem feeding in the animal kingdom.

Symbiont switching and alternative resource acquisition strategies drive mutualism breakdown.

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 in which two species cease to cooperate and mutualisms break down. What factors drive the evolutionary breakdown of mutualism? We examined the pathways toward breakdowns of the mutualism between plants and arbuscular mycorrhizal fungi. By 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 (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.

Tracking plant preference for higher-quality mycorrhizal symbionts under varying CO2 conditions over multiple generations.

The symbiosis between plants and root-colonizing arbuscular mycorrhizal (AM) fungi is one of the most ecologically important examples of interspecific cooperation in the world. AM fungi provide benefits to plants; in return plants allocate carbon resources to fungi, preferentially allocating more resources to higher-quality fungi. However, preferential allocations from plants to symbionts may vary with environmental context, particularly when resource availability affects the relative value of symbiotic services. We ask how differences in atmospheric CO 2-levels influence root colonization dynamics between AMF species that differ in their quality as symbiotic partners. We find that with increasing CO 2-conditions and over multiple plant generations, the more beneficial fungal species is able to achieve a relatively higher abundance. This suggests that increasing atmospheric carbon supply enables plants to more effectively allocate carbon to higher-quality mutualists, and over time helps reduce lower-quality AM abundance. Our results illustrate how environmental context may affect the extent to which organisms structure interactions with their mutualistic partners and have potential implications for mutualism stability and persistence under global change.

Evolutionary signals of symbiotic persistence in the legume-rhizobia mutualism.

Understanding the origins and evolutionary trajectories of symbiotic partnerships remains a major challenge. Why are some symbioses lost over evolutionary time whereas others become crucial for survival? Here, we use a quantitative trait reconstruction method to characterize different evolutionary stages in the ancient symbiosis between legumes (Fabaceae) and nitrogen-fixing bacteria, asking how labile is symbiosis across different host clades. We find that more than half of the 1,195 extant nodulating legumes analyzed have a high likelihood (>95%) of being in a state of high symbiotic persistence, meaning that they show a continued capacity to form the symbiosis over evolutionary time, even though the partnership has remained facultative and is not obligate. To explore patterns associated with the likelihood of loss and retention of the N2-fixing symbiosis, we tested for correlations between symbiotic persistence and legume distribution, climate, soil and trait data. We found a strong latitudinal effect and demonstrated that low mean annual temperatures are associated with high symbiotic persistence in legumes. Although no significant correlations between soil variables and symbiotic persistence were found, nitrogen and phosphorus leaf contents were positively correlated with legumes in a state of high symbiotic persistence. This pattern suggests that highly demanding nutrient lifestyles are associated with more stable partnerships, potentially because they "lock" the hosts into symbiotic dependency. Quantitative reconstruction methods are emerging as a powerful comparative tool to study broad patterns of symbiont loss and retention across diverse partnerships.

Order of arrival structures arbuscular mycorrhizal colonization of plants.

Priority effects - the impact of a species' arrival on subsequent community development - have been shown to influence species composition in many organisms. Whether priority effects among arbuscular mycorrhizal fungi (AMF) structure fungal root communities is not well understood. Here, we investigated whether priority effects influence the success of two closely related AMF species (Rhizophagus irregularis and Glomus aggregatum), hypothesizing that a resident AMF suppresses invader success, this effect is time-dependent and a resident will experience reduced growth when invaded. We performed two glasshouse experiments using modified pots, which permitted direct inoculation of resident and invading AMF on the roots. We quantified intraradical AMF abundances using quantitative PCR and visual colonization percentages. We found that both fungi suppressed the invading species and that this effect was strongly dependent on the time lag between inoculations. In contrast to our expectations, neither resident AMF was negatively affected by invasion. We show that order of arrival can influence the abundance of AMF species colonizing a host. These priority effects can have important implications for AMF ecology and the use of fungal inocula in sustainable agriculture.

Partner selection in the mycorrhizal mutualism.

Partner selection in the mycorrhizal symbiosis is thought to be a key factor stabilising the mutualism. Both plant hosts and mycorrhizal fungi have been shown to preferentially allocate resources to higher quality partners. This can help maintain underground cooperation, although it is likely that different plant species vary in the spatial precision with which they can select partners. Partner selection in the mycorrhizal symbiosis is presumably context-dependent and can be mediated by factors like (relative) resource abundance and resource fluctuations, competition among mycorrhizas, arrival order and cultivation history. Such factors complicate our current understanding of the importance of partner selection and its effectiveness in stimulating mutualistic cooperation.

A single evolutionary innovation drives the deep evolution of symbiotic N2-fixation in angiosperms.

Symbiotic associations occur in every habitat on earth, but we know very little about their evolutionary histories. Current models of trait evolution cannot adequately reconstruct the deep history of symbiotic innovation, because they assume homogenous evolutionary processes across millions of years. Here we use a recently developed, heterogeneous and quantitative phylogenetic framework to study the origin of the symbiosis between angiosperms and nitrogen-fixing (N2) bacterial symbionts housed in nodules. We compile the largest database of global nodulating plant species and reconstruct the symbiosis' evolution. We identify a single, cryptic evolutionary innovation driving symbiotic N2-fixation evolution, followed by multiple gains and losses of the symbiosis, and the subsequent emergence of 'stable fixers' (clades extremely unlikely to lose the symbiosis). Originating over 100 MYA, this innovation suggests deep homology in symbiotic N2-fixation. Identifying cryptic innovations on the tree of life is key to understanding the evolution of complex traits, including symbiotic partnerships.

Evolution of microbial markets.

Biological market theory has been used successfully to explain cooperative behavior in many animal species. Microbes also engage in cooperative behaviors, both with hosts and other microbes, that can be described in economic terms. However, a market approach is not traditionally used to analyze these interactions. Here, we extend the biological market framework to ask whether this theory is of use to evolutionary biologists studying microbes. We consider six economic strategies used by microbes to optimize their success in markets. We argue that an economic market framework is a useful tool to generate specific and interesting predictions about microbial interactions, including the evolution of partner discrimination, hoarding strategies, specialized versus diversified mutualistic services, and the role of spatial structures, such as flocks and consortia. There is untapped potential for studying the evolutionary dynamics of microbial systems. Market theory can help structure this potential by characterizing strategic investment of microbes across a diversity of conditions.

Analysis of a deep transcriptome from the mantle tissue of Patella vulgata Linnaeus (Mollusca: Gastropoda: Patellidae) reveals candidate biomineralising genes.

The gastropod Patella vulgata is abundant on rocky shores in Northern Europe and a significant grazer of intertidal algae. Here we report the application of Illumina sequencing to develop a transcriptome from the adult mantle tissue of P. vulgata. We obtained 47,237,104 paired-end reads of 51 bp, trialled de novo assembly methods and settled on the additive multiple K method followed by redundancy removal as resulting in the most comprehensive assembly. This yielded 29,489 contigs of at least 500 bp in length. We then used three methods to search for candidate genes relevant to biomineralisation: searches via BLAST and Hidden Markov Models for homologues of biomineralising genes from other molluscs, searches for predicted proteins containing tandem repeats and searches for secreted proteins that lacked a transmembrane domain. From the results of these searches we selected 15 contigs for verification by RT-PCR, of which 14 were successfully amplified and cloned. These included homologues of Pif-177/BSMP, Perlustrin, SPARC, AP24, Follistatin-like and Carbonic anhydrase, as well as three containing extensive G-X-Y repeats as found in nacrein. We selected two for further verification by in situ hybridisation, demonstrating expression in the larval shell field. We conclude that de novo assembly of Illumina data offers a cheap and rapid route to a predicted transcriptome that can be used as a resource for further biological study.