Evolving digital ecological networks
Miguel A. Fortuna 1,2, Luis Zaman3, Aaron P. Wagner3, Charles Ofria3
1Integrative Ecology Group, Estación Biológica de Doñana (EDB-CSIC), C/ Américo Vespucio s/n, 41092, Sevilla, Spain
2Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ, USA, 08544
3BEACON Center for the Study of Evolution in Action, Michigan State University, 567 Wilson Road Room 1441 (BPS), East Lansing, MI, USA, 48824
"It is hard to realize that the living world as we know it is just one among many possibilities".
Evolving digital ecological networks are webs of interacting, self-replicating, and evolving computer programs (i.e., digital organisms) that experience the same major ecological interactions as biological organisms (e.g., competition, predation, parasitism, and mutualism). Despite being computational, these programs evolve quickly in an open-ended way, and starting from only one or two ancestral organisms, the formation of ecological networks can be observed in real-time by tracking interactions between the constantly evolving organism phenotypes. These phenotypes may be defined by combinations of logical computations (hereafter tasks) that digital organisms perform and by expressed behaviors that have evolved. The types and outcomes of interactions between phenotypes are determined by task overlap for logic-defined phenotypes and by responses to encounters in the case of behavioral phenotypes. Biologists use these evolving networks to study active and fundamental topics within evolutionary ecology (e.g., the extent to which the architecture of multispecies networks shape coevolutionary outcomes, and the processes involved).
"So far, we have been able to study only one evolving system [...] If we want to discover generalizations about evolving systems, we will have to look at artificial ones".
In nature, species do not evolve in isolation but in large networks of interacting species (see figure 1). One of the main goals in evolutionary ecology is to disentangle the evolutionary mechanisms that shape and are shaped by patterns of interaction between species. A particularly important question concerns how coevolution, the reciprocal evolutionary change in local populations of interacting species driven by natural selection, is shaped by the architecture of food webs, plant-animal mutualistic networks, and host-parasite communities. The concept of diffuse coevolution, where adaptation is in response to a suite of biotic interactions, was the first step towards a framework unifying relevant theories in community ecology and coevolution. Understanding how individual interactions within networks influence coevolution, and conversely how coevolution influences the overall structure of networks, requires an appreciation for how pair-wise interactions change due to their broader community contexts as well as how this community context shapes selective pressures. Accordingly, research is now focusing on how reciprocal selection influences and is embedded within the structure of multispecies interactive webs, not only on particular species in isolation.
Coevolution in a community context can be addressed theoretically via mathematical modeling and simulation, by looking at ancient footprints of evolutionary history via ecological patterns that persist and are observable today, and by performing laboratory experiments with microorganisms. In spite of the long time scales involved and the substantial effort that is necessary to isolate and quantify samples, the latter approach of testing biological evolution in the lab has been successful over the last two decades. However, studying the evolution of interspecific interactions, which involves dealing with more complex webs of multiple interacting species, has proven to be a much more difficult challenge. A meta-analysis of host-phage interaction networks, carried out by Weitz and his team, found a striking statistical structure to the patterns of infection and resistance across a wide variety of environments and methods from which the hosts and phage were obtained. However, the ecological mechanisms and evolutionary processes responsible have yet to be unraveled.
Digital ecological networks enable the direct, comprehensive, and real time observation of evolving ecological interactions between antagonistic and/or mutualistic digital organisms that are difficult to study in nature. Research using self-replicating computer programs can help us understand how coevolution shapes the emergence and diversification of coevolving species interaction networks and, in turn, how changes in the overall structure of the web (e.g., through extinction of taxa or the introduction of invasive species) affect the evolution of a given species. Studying the evolution of species interaction networks in these artificial evolving systems also contributes to the development of the field, while overcoming limitations evolutionary biologists may face. For example, laboratory studies have shown that historical contingency can enable or impede the outcome of the interactions between bacteria and phage, depending on the order in which mutations occur: the phage often, but not always, evolve the ability to infect a novel host. Therefore, in order to obtain statistical power for predicting such outcomes of the coevolutionary process, experiments require a high level of replication. This stochastic nature of the evolutionary process was exemplified by Stephen Jay Gould's inquiry ("What would happen if the tape of the history of life were rewound and replayed?") Because of their ease in scalability and replication, evolving digital ecological networks open the door to experiments that incorporate this approach of replaying the tape of life. Such experiments allow researchers to quantify the role of historical contingency and repeatability in network evolution, enabling predictions about the architecture and dynamics of large networks of interacting species.
The inclusion of ecological interactions in digital systems enables new research avenues: investigations using self-replicating computer programs complement laboratory efforts by broadening the breadth of viable experiments focused on the emergence and diversification of coevolving interactions in complex communities. This cross-disciplinary research program provides fertile grounds for new collaborations between computer scientists and evolutionary biologists.
The field of digital life was inspired by the rampant computer viruses of the 1980s. These viruses were self-replicating computer programs that spread from one computer to another, but they did not evolve. Steen Rasmussen was the first to include the possibility of mutation in self-replicating computer programs by extending the once-popular Core War game, where programs competed in a digital battle ground for the computer's resources. Although Rasmussen observed some interesting evolution, mutations in this early genetic programing language produced many unstable organisms, thus prohibiting scientific experiments. Just one year later, Thomas S. Ray developed an alternative system, Tierra, and performed the first successful experiments with evolving populations of self-replicating computer programs.
Thomas S. Ray created a genetic language similar to earlier digital systems, but added several key features that made it more suitable for evolution in his artificial life system, Tierra. Primarily, he prevented instructions from writing beyond the privately allocated memory space, thus limiting the potential for organisms writing over others. The only selective pressure in Tierra was for rapid self-replication. Over the course of evolution, this pressure lead to shorter and shorter genomes, reducing the time spent copying instructions during replication. Some individuals even started executing the replication code in other organisms, allowing those "cheaters", which were originally reffered to as parasites in Ray's work, to further shrink their genetic programs. This form of cheating was the first evolved ecological interaction between organisms in artificial life software. Ray's cheaters pre-dated the formal study of evolving ecological interactions using Tierra-like digital evolution platforms by 20 years.
In 1993, Christoph Adami, Charles Ofria, and C. Titus Brown created the artificial life platform Avida at the California Institute of Technology. They added the ability for digital organisms to obtain bonus CPU cycles for performing computational tasks, like adding two numbers together. In Avida, researchers can define the available tasks and set the consequences for organisms upon successful calculation. When organisms are rewarded with additional CPU cycles, their replication rate increases. Since Avida was designed specifically as a scientific tool, it allows users to collect a comprehensive suite of data about evolving populations. Due to its flexibility and data tracking abilities, Avida has become the most widely used digital system for studying evolution. The Devolab at the BEACON Center currently continues development of Avida.
Digital organisms in Avida are self-replicating computer programs with a genome composed of assembly-like instructions. The genetic programing language in Avida contains instructions for manipulating values in registers and stacks as well as for control flow and mathematical operations. Each digital organism contains virtual hardware on which its genome is executed. To reproduce, digital organisms must copy their genome instruction by instruction (see figure 2) into a new region of memory through a potentially noisy channel that may lead to errors (i.e., mutations). While most mutations are detrimental, mutants will occasionally have higher fitness than their parents, thereby providing the basis for natural selection with all of the necessary components for Darwinian evolution. Digital organisms can acquire random binary numbers from the environment and are able to manipulate them using their genetic instructions, including the logic instruction NAND. With only this instruction, digital organisms can compute any other task by stringing together various operations because NAND is a universal logic function. If the output of processing random numbers from the environment corresponds to the result of a particular logic task, then that task is incorporated into the set of tasks the organism performs, which in turn, defines part of its phenotype.
Interactions between digital organisms occur through phenotypic matching, which, in the case of task-based phenotypes, results from the performance of overlapping logic functions (see figure 3). Different mechanisms for mapping phenotypic matching to interactions can be implemented, depending on the antagonistic or mutualistic nature of the interaction.
In host-parasite interactions, the parasite organisms benefits at the expense of the host organisms. Parasites in Avida are implemented just like other self-replicating digital organisms, but they live inside hosts and execute parasitic threads using CPU cycles stolen from their hosts. Because parasites impose a cost (lost CPU cycles) on hosts, there is selection for resistance, and when resistance starts to spread in a population, there is selective pressure for parasites to infect those new resistant hosts. Infection occurs when both the parasite and host perform at least one overlapping task. Thus a host is resistant to a particular parasite if they do not share any tasks (see figure 3). This mechanism of infection mimics the inverse-gene-for-gene model, in which infection only occurs if a host susceptibility gene (the presence of a logic task) is matched by a parasite virulence gene (a parasite performing the same task). Additional infection mechanisms, such as the matching allele and gene-for-gene models, can also be implemented.
In traditional infection genetic models, host resistance and pathogen infectivity have associated costs. These costs are an important part of theory about why defense genes do not always fix rapidly within populations. Costs are also present in digital host-parasite interactions: performing more or more complex tasks implies larger genomes and hence slower reproduction. Tasks may also allow organisms access to resources present in the abiotic environment, and the environment can be carefully manipulated to control the relative costs or benefits of resistance.
By keeping track of task-based phenotypes as well as tracking information about successful infections in the community, researchers are able to perfectly reconstruct the interaction networks of digital coevolving hosts and parasites (see figure 4). The structure of these networks is a result of the interplay between ecological processes, mainly host abundance, and coevolutionary dynamics, which lead to changes in host specificity.
Interactions in which both species obtain mutual benefit, such as those between flowering plants and pollinators, and birds and fleshy fruits, can be implemented in evolving digital experiments by following the same task matching approach used for host-parasite interactions, but using free-living organisms instead of parasitic threads. For example, one way to setup a plant-pollinator type of interaction is to use an environment containing two mutually exclusive resources: one designated for "plant" organisms and one for "pollinator" organisms. Similar to parasites attempting infection, if tasks overlap between a pollinator and a plant it visits, pollination is successful and both organisms obtain extra CPU cycles. Thus, these digital organisms obtain mutual benefit when they perform at least one common task, and more common tasks lead to larger mutual benefits. While this is one specific way to enable mutualistic interactions, many others are possible in Avida. Interactions that begin as parasitic may even evolve to be mutualistic under the right conditions. In most cases, coevolution will result in concurrent interactions between multiple phenotypes. Thus, observed networks of mutualistic interactions can inform our understanding about the outcomes and processes of coevolution in complex communities.
While host-parasite and mutualistic interactions are determined by task-based phenotypes, predator-prey interactions are determined by behavior. Predators are digital organisms that have evolved from ancestral prey phenotypes to locate, attack, and consume organisms. When a predator executes an attack instruction (acquired through mutation), it kills a neighboring organism. When predators kill prey, they gain resources required for reproduction (e.g., CPU cycles) proportional to the level accumulated by the consumed prey. Selection favors behavioral strategies in prey that enable them to avoid being eaten. At the same time, selection favors predators with behavioral strategies that improve their food finding and prey attacking abilities. The resulting diversity in the continuously evolving behavioral phenotypes creates dynamic predator-prey interaction networks in which selective forces are constantly changing as a consequence of the emergence of new, and loss of old, behaviors. Because predators and prey move around in and use information about their environment, these experiments are typically carried out using spatially structured populations. On the other hand, host-parasite and mutualistic coevolution are often done in well-mixed environments, though the choice of the environment is at the discretion of the experimenter.
Understanding how biodiversity is organized in natural ecosystems requires going beyond the study of pairs of interacting species. Using digital organisms, one can find generalities about the evolutionary and ecological processes shaping the web of interactions among species, as well as the coevolutionary processes embedded within these networks. By tracing the evolution of digital communities and their ecological networks, researchers obtain perfect fossil records of how the number and patterns of links among interacting phenotypes evolved.
The stability-diversity debate is a long-standing debate about whether more diverse ecological networks are also more stable. Until recently, this debate has focused on one component of biodiversity: species diversity. However, newer research has begun dealing with another component of biodiversity: diversity in species interactions. Mathematical models show that a mixture of antagonistic and mutualistic interactions can stabilize population dynamics and that the loss of one interaction type may critically destabilize ecosystems. Studies with digital organisms can shed light on this debate from an empirical perspective because the types of interactions included can be manipulated and the stability of the resulting evolving digital ecological network can be measured.
Equally addressable using evolving digital ecological networks are many of the open questions concerning the coevolution of ecological interactions in multispecies communities. For example, do coevolutionary dynamics change as communities become richer? Is there any limit to their richness? Is the evolution of interactions between multispecies networks historically contingent? Why do some ecological scenarios lead to predictable network structures and others do not? Do genetic constraints play a large role in the evolution of ecological networks? These are only a few of many open questions concerning the coevolution of ecological interactions in multispecies communities.
These and many related questions require researchers to look across the evolutionary history of ecological network formation. For natural systems, those data are very difficult to collect. With digital organisms, watching both the coevolutionary process and ecological network formation is possible in real time. Data on the abundance of interacting phenotypes are recorded without error, hence the evolutionary implications of ecological processes can be explored in-depth.
The study of self-replicating and evolving computer programs offers a tantalizing glimpse into the evolution of interactions among organisms that do not share any ancestry with biochemical life of Earth. This comes with potential caveats in translating predictions of evolving digital networks to biological ones because mechanistic details differ substantially between interacting digital organisms and interacting biological organisms. Nevertheless, these digital networks contain the necessary components for ongoing coevolutionary dynamics in large webs of interacting organisms. In spite of the differences between biological and digital evolution, the study of evolving digital ecological networks can lead to a more predictive understanding of natural dynamics. Because the general operational processes (e.g., Darwinian evolution, mutualism, parasitism) do not differ, studies utilizing digital networks can uncover rules operating on and within ecological networks. Together with microbial experiments, they create opportunities for furthering the understanding of the interplay between ecological and evolutionary processes among interacting species.
We thank Simon A. Levin, Jordi Bascompte, Justin Meyer and other members of the BEACON Center, for useful discussions, comments and suggestions that have contributed to the initial development of the manuscript. We very much appreciate the thoughtful and constructive evaluations by Joshua Weitz and Chris Adami that have improved the clarity and readability of this topic page. This work was funded by a Marie Curie International Outgoing Fellowship within the European Commission's 7th Framework Programme (to M.A.F.), an AT&T Research Labs Fellowship (to L.Z.), and funding from the BEACON Center and iCER (to A.P.W. and C.O.).
This material is based in part upon work supported by the National Science Foundation under Cooperative Agreement No. DBI-0939454. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation.
- ^ F Jacob (1977) Evolution and tinkering. Science 196:1161-6
- ^ Kritsky G (1991) Darwin's Madagascan Hawk Moth prediction. American Entomologist 37: 206-209.
- ^ J M Smith (1992) Evolutionary biology. Byte-sized evolution. Nature 355:772-3
- ^ David M Post, Eric P Palkovacs (2009) Eco-evolutionary feedbacks in community and ecosystem ecology: interactions between the ecological theatre and the evolutionary play. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 364:1629-40
- ^ a b John N Thompson (2009) The coevolving web of life. Am. Nat. 173:125-40
- ^ Thomas W Schoener (2011) The newest synthesis: understanding the interplay of evolutionary and ecological dynamics. Science 331:426-9
- ^ J N Thompson (1999) The evolution of species interactions. Science 284:2116-8
- ^ Janzen, D. H. (1990). When is it coevolution? Evolution 34: 611-612.
- ^ Fox, L. R. (1988). Diffuse coevolution within complex communities. Ecology 69: 906-907.
- ^ Thompson, J. N. (1994). The coevolutionary process. University of Chicago Press.
- ^ Jeremy B Yoder, Scott L Nuismer (2010) When does coevolution promote diversification? Am. Nat. 176:802-17
- ^ R Tucker Gilman, Scott L Nuismer, Dwueng-Chwuan Jhwueng (2012) Coevolution in multidimensional trait space favours escape from parasites and pathogens. Nature 483:328-30
- ^ Enrico L Rezende, Jessica E Lavabre, Paulo R Guimarães, Pedro Jordano, Jordi Bascompte (2007) Non-random coextinctions in phylogenetically structured mutualistic networks. Nature 448:925-8
- ^ José M Gómez, Miguel Verdú, Francisco Perfectti (2010) Ecological interactions are evolutionarily conserved across the entire tree of life. Nature 465:918-21
- ^ Bohannan BJM, Lenski RE (2000) Linking genetic change to community evolution: insights from studies of bacteria and bacteriophage. Ecology Letters 3: 362-377.
- ^ R E Lenski, M Travisano (1994) Dynamics of adaptation and diversification: a 10,000-generation experiment with bacterial populations. Proc. Natl. Acad. Sci. U.S.A. 91:6808-14
- ^ Cesar O Flores, Justin R Meyer, Sergi Valverde, Lauren Farr, Joshua S Weitz (2011) Statistical structure of host-phage interactions. Proc. Natl. Acad. Sci. U.S.A. 108:E288-97
- ^ Justin R Meyer, Devin T Dobias, Joshua S Weitz, Jeffrey E Barrick, Ryan T Quick, Richard E Lenski (2012) Repeatability and contingency in the evolution of a key innovation in phage lambda. Science 335:428-32
- ^ Gould SJ (1990) Wonderful life: the Burgess Shale and the nature of history. W. W. Norton.
- ^ Rasmussen S, Knudsen C, Feldberg R, Hindsholm M (1990) The coreworld: emergence and evolution of cooperative structures in a computational chemistry. Physica D 75: 1-3.
- ^ a b Ray TS (1992) An approach to the synthesis of life. In Langton CG, Taylor C, Farmer JD, Rasmussen S, editors. Proceedings of Artificial Life II: pp. 371-408.
- ^ a b Avida download page (WebCite archive)
- ^ a b Charles Ofria, Claus O Wilke (2004) Avida: a software platform for research in computational evolutionary biology. Artif. Life 10:191-229
- ^ Devolab
- ^ R E Lenski, C Ofria, T C Collier, C Adami (1999) Genome complexity, robustness and genetic interactions in digital organisms. Nature 400:661-4
- ^ Zaman, L., Devangam, S, Ofria, C. (2011). Rapid host-parasite coevolution drives the production and maintenance of diversity in digital organisms. Proceedings of the 13th Annual Conference on Genetic and Evolutionary Computation (GECCO), 219-226.
- ^ Andrew Fenton, Janis Antonovics, Michael A Brockhurst (2009) Inverse-gene-for-gene infection genetics and coevolutionary dynamics. Am. Nat. 174:E230-42
- ^ Agrawal, A. and Lively, C. M. (2002). Infection genetics: gene-for-gene versus matching-alleles models an all points in between. Evolutionary Ecology Research, 4: 79-90.
- ^ Bohannan BJM, Lenski RE (2000) Linking genetic change to community evolution: insights from studies of bacteria and bacteriophage. Ecology Letters 3: 362-377.
- ^ Robert Poulin (2010) Network analysis shining light on parasite ecology and diversity. Trends Parasitol. 26:492-8
- ^ Pajek Wiki Homepage (WebCite copy).
- ^ Paulo R Guimarães, Pedro Jordano, John N Thompson (2011) Evolution and coevolution in mutualistic networks. Ecol. Lett. 14:877-85
- ^ K S McCann (2000) The diversity-stability debate. Nature 405:228-33
- ^ A Mougi, M Kondoh (2012) Diversity of interaction types and ecological community stability. Science 337:349-51
- ^ Elisa Thébault, Colin Fontaine (2010) Stability of ecological communities and the architecture of mutualistic and trophic networks. Science 329:853-6
- ^ Institute for Cyber Enabled Research (WebCite copy).