Environment, Development, and Evolution Toward a New Evolutionary Synthesis
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11 Environment, Development, and Evolution Toward a New Evolutionary Synthesis In my opinion, the greatest error which I have committed, has not been allowing sufficient weight to the direct action of the environment, i.e. food, climate, etc., independently of natural selection. Charles Darwin to Moritz Wagner, 1876 May your symbionts be with you. Angela Douglas, 2010 To develop is to interact with the environment. To evolve is to alter these interactions in a heritable manner. Armin Moczek, 2015 he importance of development for evolutionary biology is not limited to the role of developmental regulatory genes discussed in Chapter T10. The studies of developmental plasticity and developmental sym- biosis point to something quite unexpected in evolutionary theory: that the environment not only selects variation, it helps construct and shape varia- tion. This integration of ecological developmental biology into evolutionary biology has sometimes been referred to as ecological evolutionary devel- opmental biology, or “eco-evo-devo.” Eco-evo-devo has several research projects, but its main goal, as recently stated (Abouheif et al. 2014) is to “uncover the rules that underlie the interactions between an organism’s environment, genes, and development and to incorporate these rules into evolutionary theory.” ©2015 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured or disseminated in any form without express written permission from the publisher. 436 Chapter 11 With the application of knowledge gained from the studies now being done in ecological developmental biology, a new and more inclusive evo- lutionary theory is being forged. So far, eco-devo has contributed at least three components to this nascent evolutionary synthesis. These are the three concepts introduced in the first section of the textbook. The first concept introduced into evolutionary biology is developmental plasticity. This concept forms the basis of genetic accommodation, the idea that en- vironmentally induced changes to a phenotype, when adaptive over long periods of time, can become the genetic norm for a species. Developmental plasticity is also the basis of niche construction, wherein the developing organism can modify its environment because there are plastic features in its habitat. Second, eco-devo has maintained that epigenetic inheritance systems, such as the epialleles formed by environmental agents, are also important sources of selectable variation. The third of these is the con- cept of developmental symbiosis. Symbiosis has given rise to processes of symbiont-mediated evolution, including the possibility that the holobiont is a unit of evolutionary selection. Thus, what is added to evolutionary biology are the agencies of the environment (see Moczek 2015). These fac- tors had been hypothesized to be exceptions to the general rules of nature, and thus were only minor areas of evolutionary theory. Now, these same factors are seen as being pervasive throughout nature, even characteristics of natural life on this planet. They therefore need to be incorporated into an extended theory of evolution. The above-mentioned discoveries of eco-evo-devo have allowed evo- lutionary biology to expand beyond the constraints of the following four assumptions of the Modern Synthesis: 1. “Genetic variation in alleles is the only evolutionarily relevant variation.” Ecological developmental biology demonstrates that epigenetic variation can also be transmitted from generation to generation, can have profound phenotypic consequences, and therefore consti- tutes an important component of selectable variation. 2. “Individual genotypes are the main target of selection.” Ecological devel- opmental biology shows that organisms may be more like ecosys- tems, holobionts composed of numerous genotypes that interact with each other. This may allow natural selection to favor “teams” rather than particular individuals and may also privilege “relation- ships” as a unit of selection. 3. “The environment is a selective agent of phenotypes but is of no conse- quence in producing the phenotype.” Ecological developmental biol- ogy has shown that developing organisms respond to environmen- tal conditions by altering which phenotypes they produce and that environmental agents help generate particular phenotypes. 4. “The environment is a given and is unchanged by the organism being selected.” Ecological developmental biology finds that organisms reciprocally shape their immediate environment in ways that match their traits. The environment is altered by the organisms as they develop. ©2015 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured or disseminated in any form without express written permission from the publisher. Environment, Development, and Evolution 437 Symbiotic Inheritance There are several ways that symbiotic inheritance is extremely important for evolution. As described in Chapter 3, the holobiont may be the unit of natural selection (Margulis and Fester 1991; Sapp 1994; Margulis 1999; Douglas 2010; Gilbert et al. 2010, 2012; McFall-Ngai et al. 2013). In addi- tion, developmental symbiosis may be critical for several evolutionary processes, including: • The production of new selectable variation. This is the result of symbiopoiesis, wherein the symbiont is part of the developmen- tal interactions that generate the holobiont. • The alteration of genomes, constraining and permitting certain ecological ranges • Reproductive isolation, potentiating new species • The formation of new types of cells. This can be accomplished by symbiogenesis, the acquisition of new genetic material from other organisms into the cell’s inheritance systems. • Evolutionary transitions such as those enabling multicellular life and the origins of complex ecosystems Holobiont variation produced by symbionts Symbionts can be passed from generation to generation. Alleles in these symbionts can alter the phenotype of the holobiont and lead to selection of the holobiont based on the alleles of the symbiont. One example of symbi- onts conferring variation to the entire organism involves pea aphids and their symbiotic bacteria. The pea aphid Acyrthosiphon pisum and its bacte- rial symbiont Buchnera aphidicola have a mutually obligate symbiosis. That is, neither the aphids nor the bacteria will flourish without their partner. Pea aphids rely on B. aphidicola to provide essential amino acids that are absent from the pea aphids’ phloem sap diet (Baumann 2005). In exchange, the pea aphids supply nutrients and intracellular niches that permit the B. aphidicola to reproduce (Soler et al. 2001). These bacteria live inside the cells of the aphids (and are therefore called endosymbionts). Because of this interdependence, the aphids are highly constrained to the ecological tolerances of B. aphidicola (Dunbar 2007). Buchnera aphidicola provides more than essential amino acids, though. Certain strains of B. aphidicola can give thermotolerance to the holobiont. The heat tolerance of pea aphids and B. aphidicola is abrogated by a single nucleotide deletion in the promoter of the heat-shock gene ibpA. This mi- crobial gene encodes a small heat-shock protein, and the deletion eliminates the transcriptional response of ibpA to heat (Dunbar et al. 2007). In other words, the thermotolerance phenotype of the holobiont depends upon the regulatory allele of the symbiont. Only those aphids containing the wild- type Buchnera can produce offspring at high temperatures. Although pea aphids harboring B. aphidicola with the short ibpA promoter allele suffer from decreased thermotolerance, they experience increased reproductive ©2015 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured or disseminated in any form without express written permission from the publisher. 438 Chapter 11 Figure 11.1 Fecundity (number of offspring 9 5A-long per day) of the pea aphid Acyrthosiphon pisum 8 depends upon the temperature at which the ju- 5A-short venile is raised. Those aphids whose Buchnera 7 aphidicola symbionts have the wild-type allele 6 (5A-long) for this heat-shock protein have slightly lower fecundity at most temperatures but can 5 have fecundity at high temperatures, whereas those aphids carrying symbionts with the mu- 4 tant allele (5A-short) do not. (After Dunbar et Daily fecundity 3 al. 2007.) 2 1 0 15 20 25 27 30 35 38 Temperature treatment (°C) rates under cooler temperatures (15°C–20°C). Aphid lines containing the short-promoter B. aphidicola produce more offspring per day during the first 6 days of reproduction compared with aphid lines containing long- allele B. aphidicola (Figure 11.1). This trade-off between thermotolerance and fecundity allows the pea aphids and B. aphidicola to diversify. Moran and Yun (2015), taking advantage of the maternal inheritance of B. aphidocola, were able to replace a heat-sensitive strain of Buchnera with a thermotolerant strain (thus disrupting 100 million years of continuous maternal transmission in its hosts!). The new symbionts were stably trans- mitted, and the aphids with the new, thermotolerant Buchnera displayed a dramatic increase in heat tolerance. This directly demonstrated that the symbiontGilbert genotype Epel 2e has a strong effect on holobiont fitness and ecology. Sinauer Associates Such partnerships,Morales Studio where thermotolerance is provided by the symbiont, are alsoGilbert_Epel2e_11.01.ai seen in coral and Christmas 03-20-15 cactuses* (see Gilbert et al. 2010). Another bacterial symbiont