Journal of Theoretical Biology 437 (2018) 137–140

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Biological novelty in the anthropocene Marcelino Fuentes Facultade de Ciencias, Universidade da Coruña, A Coruña, 15071 Spain

a r t i c l e

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Article history: Received 22 September 2016 Revised 6 September 2017 Accepted 23 October 2017 Available online 26 October 2017 Keywords: Cooperation Ecosystems Evolution Inheritance Human ecology

a b s t r a c t It is well known that humans are creating new variants of organisms, ecosystems and landscapes. Here I argue that the degree of biological novelty generated by humans goes deeper than that. We use property rules to create exclusivity in cooperation among humans, and between humans and other biological entities, thus overcoming social dilemmas and breaking barriers to cooperation. This is leading to novel forms of cooperation. One of them is the human control, modification and replication of whole ecosystems. For the first time, there exist ecosystems with functional design, division of labor and unlimited heredity. We use mental representation and language as new mechanisms of inheritance and modification that apply to an increasing variety of biological and non-biological entities. As a result, the speed, depth and scale of biological innovation are unprecedented in the history of life. © 2017 Elsevier Ltd. All rights reserved.

1. Introduction Humans are transforming the Earth’s surface, the atmosphere and the biosphere. We are changing landscapes, increasing the concentration of CO2 and other gases, and reorganizing the Earth’s biota (Crutzen, 2006; Steffen et al., 2007). The human domination of the biosphere is often portrayed as a destructive process — humans extinguish species, replace unique habitats and species assemblages with common ones, and generally impoverish the Earth’s biological wealth (McKinney & Lockwood, 1999; Olden et al., 2004; Butchart et al., 2010; Pereira et al., 2010; Barnosky et al., 2011; Burger et al., 2012; Dirzo et al., 2014; Pimm et al., 2014). Here I analyze the role of humans as a creative force. Previous studies have noted that humans are creating new organismal variants, species, communities, ecosystems, landscapes and biomes (Rosenzweig, 2003; Palmer et al., 2004; Hobbs et al., 2006; Ellis & Ramankutty, 2008; Thomas, 2013a, 2013b, 2015; 2017; Ellis, 2015). But the biological novelty produced by humans goes deeper. Humans are creating a new form of inheritance based on the human capacity for communication and information storage (Jablonka and Lamb, 2005), and new forms of biological cooperation and division of labor that are unprecedented in kind, intensity and extent. 2. New forms of cooperation At least some degree of exclusivity is necessary for cooperation and mutualism to take place (Queller, 1997; Leigh 2010). Cooperators and mutualists must keep a sufficiently large portion of the fruits of their collaboration for themselves or their kin, and away E-mail address: [email protected] https://doi.org/10.1016/j.jtbi.2017.10.027 0022-5193/© 2017 Elsevier Ltd. All rights reserved.

from free riders. In the origin of eukaryotes, an initially independent organism physically enclosed another one, thus both enjoying almost exclusive access to the benefits of their association. Cooperation within multicellular bodies involves the permanent physical attachment of cells and the exclusion of foreign cells by organic barriers and the immune system. Eusocial colonies use kin recognition systems that involve frequent physical or chemical contact to exclude non-kin from the fruits of colony work. No biological cooperation system is completely immune to free riders and intruders, but all the examples above succeeded in finding new ways to exclude enough of them to make new forms of cooperation profitable (Maynard Smith and Száthmary, 1995; Queller, 1997; Szathmáry, 2015). The key to cooperation among humans and between humans and other biological entities is the exclusivity provided by property rights. Property rules establish who can do what with each resource. They include any explicit or implicit social norm that delineates the access of each human or group of humans to objects and their attributes (Barzel, 1997). Implicit in this definition is the power of property rules to exclude certain people from using or enjoying objects and their attributes. Individual private property became more beneficial and less costly during the transition from hunting-foraging to farming, and now governs a large share of human life (Bowles and Choi, 2013; Gallagher et al., 2015). Individual private property often encourages intensive labor and investment, including those necessary to sustain many mutualisms between humans and other organisms. However, property rules also apply to communal resources, both by excluding outsiders and by delineating use by commoners. Communal property rules can sometimes generate proper incentives and sustain high levels of cooperation (Ostrom, 1990). Much of the early domestication of animals

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and plants and the origin of farming took place in communal settings. Property rights will exist only when most people, most of the time, peacefully adhere to them instead of engaging in costly conflicts over resource use. Some non-human organisms, including those that practice farming, often follow a simple property rule of territorial incumbency (Gintis, 2007; Strassmann and Queller, 2014). Humans use cognitive abilities and moral emotions to collectively devise, fine-tune, accept and enforce property rules that apply to a wide range of objects, are tailored for long-term goals and for specific circumstances, help to elicit information, and minimize conflict (Powers and Lehman, 2013; Powers et al., 2016). Our more comprehensive rules enable better coordination and cooperation. We lack the cognitive ability, the information and the moral disposition to create a perfect system of property rules that maximizes human cooperation and welfare (Barzel, 1997; Allen, 20 0 0). But some of the imperfect ones we have created have unleashed a revolution in cooperation. The collective enforcement of property rules in humans is at least in part explained by our unique cognitive and emotional abilities allowing for simple reciprocity. These abilities include those related to gathering, analyzing and sharing information on one’s and others’ cooperation successes and failures, and to controlling one’s short-sighted impulses so as to reap the long-term benefits of reputation. It has been argued that, although self-interested cognitive abilities and forward-looking self-control may be enough to sustain cooperation in repeated dyadic and small-group interactions, the success of social norms, including property rights, in promoting cooperation in large groups where we often interact with strangers requires strong reciprocity – punishing defectors and abstaining from free riding, conditional on the behavior of others, when to do so is costly in the long run for the agent or its kin (Gintis, 20 0 0; Fehr and Fischbacher, 2003; see Bowles (2004) and Carvalho and Koyama (2010) for the case of the emergence of markets; and see Binmore, 2006; Guala, 2012; Burton-Chellew and West, 2013; Powers et al., 2016 for skeptical views). By conferring some degree of exclusivity to a human individual or group over some resource, property rules expand the range of actions that a human or group of humans can expect to undertake with a profit. For example, property rules allow a farmer or community of farmers to enjoy relatively exclusive access to the benefits of their association with the animals, plants, fungi and bacteria that provide them with food and clothes. Farming does not develop when the lack of property rights allows other unauthorized humans to reap the benefits derived from the efforts and sacrifices of the farmers. Property rights can exclude other humans, but not other organisms, such as pests or predators, that threaten to take away those benefits. However, property rights encourage the farmers to invest in devices, such as fences or pesticides, that partially exclude undesired organisms in the expectation that they, and no other humans, will profit from that exclusion. Fences and pesticides play the same role in the association of humans and other biological entities as, for example, skins and antibodies do in multicellular organisms. Collective enforcement of property rights allows for the physical separation of property right holders and their property. Humans are unique in achieving a large degree of exclusivity while not being permanently attached to their property, as exemplified by contracts of usufruct, lending, firm organization, credit, futures, or insurance. Again, this expands the range of conditions where we humans can successfully cooperate among ourselves and associate with other biological entities. Property rights allow the development of markets. In markets, humans exchange non-human biological entities at little cost. While in eukaryotic cells, for example, mitochondria are almost always transmitted from mothers to offspring, in the human mar-

ket entities from amino acids and DNA sequences to populations and ecosystems can change owners without the constraint of descent. As a result, a human, either individually or in association with other humans, can build efficient combinations of biological entities instead of just inheriting fixed ones. Another advantage of markets is that most humans do not cooperate with other biological entities for the direct enjoyment of the products of the association, but to share these with other humans in exchange for other goods. The decoupling of property rights and physical attachment, and the possibility of exchange both contribute to an unprecedented extent and depth of division of labor. 3. Division of labor We allocate biological entities under our control to different tasks according to their relative efficiency. For example, traditional farmers assign plants, cattle, chicken, dogs, cats, bees, and fermenting yeasts and bacteria, as well as fields, woods, ponds and other ecosystem types, to different functions. The production of some modern vaccines involves the coordinated work of humans, laboratory mice, bacteria, viruses and tobacco plants, each performing a different task (Yusibov et al., 2013). We choose biological entities that are well suited for each task, and in addition we purposely modify and combine these entities to further improve their performance and their complementarity. Artificial selection, hybridization, genetic engineering and synthetic biology are producing an explosion of new biodiversity (Rieseberg and Carney, 1998; Drake and Klingenberg, 2010; Moreno, 2012; Redford et al., 2013). Similarly, we create novel ecological communities, ecosystems and biomes to better provide us with specialized ecosystem services (Rosenzweig, 2003; Palmer et al., 2004; Hobbs et al., 2006; Ellis, 2015). Property rights and markets allow for some people to specialize on biological modification (for example, working in research organizations or biotechnology firms), while others, like farmers or physicians, use the products of the former and specialize on other tasks. Biological entities modified by humans increase their performance for the chosen tasks, but, due to trade-offs, lose performance in other tasks. In many cases, the modified entities even lose some or all their capacity to replicate without human intervention. Limited replication occurs for a variety of reasons. First, humans use a fraction of a dominated population for producing goods and services, and set aside another fraction for producing the next generation. This is the case of many domestic populations that are artificially sorted into reproductive and non-reproductive fractions. A particular case of this happens when part of the population produces the next generation and another part produces eggs or juveniles that are used for human consumption. And to some extent it is also the case of wild populations that are artificially sorted into harvestable and non-harvestable subpopulations. Some non-human organisms, such as ants or amoebae that practice rudimentary farming, also exert demographic control to enhance long-term harvest (Mueller et al., 2005; Brock et al., 2011). But humans take demographic control to the extreme (Fuentes, 2014), as secure property rights allow for investing with longer time horizons, and as we use our cognitive abilities, our division of labor and the market price system to better manipulate biotic and abiotic variables to adjust resource populations to changes in the environment and in human demand. Second, some human-modified biological entities can reproduce within human-dominated ecosystems but have lost adaptations that would allow them to reproduce outside them. Examples are some dog breeds, many farm animals and plants, and obligate commensals of humans such as house sparrows, pigeons and some geckos.

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And third, some human-manipulated biological entities do not replicate at all by themselves and only occur with human intervention. Examples are some hybrids such as mules, plants that are designed to be sterile to aid in the production of hybrids (as in some varieties of rice) or because seeds are undesirable (as in domestic bananas), fish that are designed to be sterile to avoid their spread outside aquaculture operations, sterile mosquitoes that are produced to eradicate natural ones, and some attenuated viruses that are used as vaccines. 4. A new inheritance system Humans use mental representation, language and institutions to store, transmit, translate and modify biological information. Before humans the information needed to generate a nucleotide sequence resided almost exclusively on a previous nucleotide sequence. Now it also resides in human minds and words, or is implicit in human morals and laws. It is stored in neural circuits, papers and computers, and in disperse collections of any of these substrates (Jablonka and Lamb, 2005). Humans can copy information between different substrates. We can sequence DNA using physical or chemical signals, then memorize sequences in our brains, write them on paper or store them in a computer, and finally copy them back to DNA (Gillings and Westoby, 2014). This unties inheritance of DNA sequences from parentage and from narrow organic processes in general. We use artificial means of inheritance to replicate not only molecules, cells and organisms, but also abiotic environments, population and community structures, and ecosystems. Humans can predict phenotypes from genetic information. Natural selection acts on existing, organic variants that arise by random mutation and recombination. In contrast, humans design biological entities before they exist, saving the effort of building those that we predict would be useless (Jablonka and Lamb, 2005). In other words, thanks to inheritance via human minds we generate variants that are biased towards human utility instead of being random. This accelerates the rate of biological evolution. 5. New ecosystems Humans control, modify and replicate whole ecosystems. Thanks to artificial systems of information we create ecosystems with inheritance and design, and we are the first species to generate division of labor among ecosystems. Deliberate human planning and execution, as well as unintended effects of human decisions and collective behaviors, are mechanisms of inheritance that produce replicates of ecosystems. Often, the species composition and abundance, soil characteristics, water and nutrient inputs and outputs, and other traits of a human-dominated ecosystem are replicated following an instruction set that is not dispersed throughout the components (the soma) of the ecosystem, but concentrated in humans, either individually or collectively (Jablonka and Lamb, 2005; Zeder, 2016). To some extent this is also true of ecosystem engineering by beavers that build dams or ants that tend fungus gardens (Jones et al., 1994), and of niche construction in general (Odling-Smee et al., 2003; Zeder, 2016). However, it seems that ecosystems engineered or constructed by these organisms have "limited heredity" (Maynard Smith and Száthmary, 1995), which allows the specification of a small variety of ecosystem types (Odling-Smee et al., 2003), while human-dominated ecosystems have "unlimited heredity" (Maynard Smith and Szathmáry, 1995), in the sense that we can design and specify many more types of ecosystems than we can actually build due to space or other limitations. Unlike other ecosystem engineers, humans create different kinds of ecosystems to perform different tasks and to complement

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each other. For example, fish farms use inputs from agricultural farms, and these in turn use inputs from tree plantations. Many human-dominated ecosystems have functional boundaries. They are physically separated among them and from natural ecosystems. Extreme examples are greenhouses, culture chambers, some traditional farms, fish farms, waste water treatment plants, and in vitro ecosystems. Sometimes, separation is planned by individual humans to serve an ecological function. For example, a farmer may keep several greenhouses, each planted with different species, within his or her property, or may build a fence to protect his or her livestock from carnivores. Other times, boundaries separate properties of different humans, and thus result from human institutions. Boundaries of human-dominated ecosystems often serve one of the functions that external membranes and skeletons play in cells and multicellular organisms - to exclude non-cooperators from the benefits of cooperation. An important difference is that boundaries need not be continuous to play this role. Thanks to property rights, individual humans and groups of humans can own non-contiguous resources and still effectively exclude other humans. Either because different ecosystems are owned by the same people or because different owners cooperate with one another, human-dominated ecosystems can cooperate even if they are not contiguous. Thanks to artificial transport and communication, we can divide labor and exchange resources, organisms and information among ecosystems that are thousands of kilometers away. Lastly, the human transformation of ecosystems differs quantitatively from that by other ecosystem engineers. The change in species composition, the demographic control and protection of resource populations, the magnitude of evolutionary transformation, the biodiversity created, the control of the abiotic environment, and the spatial extent of transformation are all unprecedented (Ellis, 2015). The network of human-based cooperation now encompasses a large portion of the biosphere (Vitousek et al., 1997; Ellis, 2015). Humans and domestic vertebrates make up more than 95% of the terrestrial vertebrate biomass, and humans appropriate about 25% of terrestrial primary productivity (Smil, 2011). Human planning also extends to wild ecosystems, as exemplified by reintroductions of extinct populations, protection of endangered populations from enemies, control of invasive organisms, culling, and fire management. Acknowledgements I thank an anonymous reviewer for comments on the manuscript. I was funded by grant GRC2014/050 (Grupo de Investigación en Biología Evolutiva) from the Government of Galicia (Spain). References Allen, D.W., 20 0 0. Transaction costs. In: Bouckaert, B., de Geest, G. (Eds.), Encyclopedia of Law and Economics. Edward Elgar Press, Cheltenham, UK, pp. 893–926. Barnosky, A.D., Matzke, N., Tomiya, S., Wogan, G.O., Swartz, B., Quental, T.B., Marshall, C., McGuire, J.L., Lindsey, E.L., Maguire, K.C., 2011. Has the Earth’s sixth mass extinction already arrived? Nature 471, 51–57. Barzel, Y., 1997. Economic Analysis of Property Rights, 2nd Cambridge University Press, Cambridge, UK. Binmore, K., 2006. Why do people cooperate? Politics Philos. Econ. 5, 81–96. Bowles, S., 2004. Microeconomics: Behavior, Institutions, and Evolution. Princeton University Press, Princeton, NJ, USA. Bowles, S., Choi, J.K., 2013. Coevolution of farming and private property during the early Holocene. Proc. Natl. Acad. Sci. U.S.A. 110, 8830–8835. Brock, D.A., Douglas, T.E., Queller, D.C., Strassmann, J.E., 2011. Primitive agriculture in a social amoeba. Nature 469, 393. Burger, J.R., Allen, C.D., Brown, J.H., Burnside, W.R., Davidson, A.D., Fristoe, T.S., Hamilton, M.J., Mercado-Silva, N., Nekola, J.C., Okie, J.G., 2012. The macroecology of sustainability. PLoS Biol. 10, e1001345. Burton-Chellew, M.N., West, S.A., 2013. Prosocial preferences do not explain human cooperation in public-goods games. Proc. Natl. Acad. Sci. U. S. A. 110, 216–221.

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