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The Union of Ecology and Evolution: Extended Phenotypes and Community Genetics

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The Union of Ecology and Evolution: Extended Phenotypes and Community Genetics Viewpoint The Union of Ecology and Evolution: Extended Phenotypes and Community Genetics JEFFRY B. MITTON ooking back over the last four Community genetics relies on genes hybridization between cottonwood Ldecades, I can see several eras, or with extended phenotypes and on com- species in Utah and between Eucalyptus pulses of activity, in evolutionary bio- munity heritability. An extended phe- species in Australia convincingly estab- logy. The use of protein electrophoresis notype (Dawkins 1982) is a genetically lished that insect herbivores respond to from the 1960s onward exposed all based consequence that extends beyond the blending and segregation of plant species to genetic analysis and initiated the physical boundaries of the organ- defensive chemicals in hybrid zones. a long-running controversy over ism bearing the gene. For example, a Both the abundance and the diversity of whether most alleles are subject to se- cross between Populus fremontii and P. insect herbivores are elevated in tree hy- lection. Then, starting in the 1970s, evo- angustifolia exhibits genetic variation at brid zones. The enhanced communities lutionary biologists adopted DNA se- one locus that increases the level of of herbivorous insects on hybrid and quencing techniques, which fueled the condensed tannin tenfold. Tannin, a backcross trees constitute the extended growth of molecular systematics. More chemical plant defense, influences the phenotypes. recently, markers from mitochondrial behavior of herbivorous insects and the Community heritability of extended DNA and then chloroplast DNA have rate at which leaves decompose. Thus, a phenotypes was demonstrated in an ex- provided the data for phylogeography, cottonwood’s extended phenotype in- perimental garden planted with the geographic analyses of phylogenetic cludes herbivore density and diversity progeny of controlled crosses involving lineages that make inferences about and the rate of nutrient cycling in de- Eucalyptus amygdelina and E. risdonii. glacial refugia, range expansions, and composing leaves. The principle of In both natural populations and the ex- other important features of species’ community heritability is attributed to perimental garden, each parental evolutionary history. A paper published Goodnight (1990), who wrote, “If the species has its own community of in- in Ecology (Whitham et al. 2003) may interactions among the members of the sects, but their hybrids sustain both in- herald a new era in evolutionary biol- community are passed intact from the sect communities. The densities of her- ogy: the elaboration of community and ‘parent’ community to the ‘offspring’ bivorous insects are much higher on ecosystem genetics. If this comes about, community, the interaction will be her- hybrid and backcross genotypes, and evolutionary biology and ecology will itable at the community level.” some insects are abundant within hy- be more tightly linked than ever before. The basis of community genetics is brid zones and rare outside them. As a population geneticist who usu- intraspecific genetic variation with ma- The notion of extended phenotypes ally focuses on single-locus studies of jor effects that trigger a cascade of inter- triggering interactions that ripple variation within species, the sound of actions with other species in the com- through a community has some prece- community and ecosystem genetics ini- munity. Other fields of genetics focus dent in the literature. Claude Combes, tially made me fidgety. It reminded me on indivduals or make use of neutral in his treatment of the ecology and evo- of the notion of cultural evolution, a genetic variation to study systematics, lution of intimate interactions (2001), short-lived metaphoric extension of to infer historic events, or to measure repeatedly refers to the extended phe- evolutionary principles to language, gene flow. Because the genetic variation notypes of parasites. His examples in- technical innovations, fashion, and underlying the extended phenotype clude the modifications of physiology, fads. But community genetics is intro- conforms to normal patterns of inheri- development, and behavior that make duced here with well-documented tance, the extended phenotypes—the the host a more suitable environment empirical studies of genetic variation interactions with other species—are for the parasite and improve the host’s that produces not only phenotypic vari- heritable. performance as a vector. For example, ation within a species but also changes The most engaging aspect of this pa- diarrhea is seen not just as an inconse- in interactions among species that are per is that it was inspired by, and its pre- quential symptom of parasitism but as profound in effect and widespread in a sentation is based on, empirical studies. an extended phenotype that improves community. For example, studies of zones of the dispersal of larvae or cysts. 208 BioScience • March 2003 / Vol. 53 No. 3 Viewpoint One of my favorite examples of an the community; when infected deer phenotypes. This will be a tiny number extended phenotype is the germ war- move into an area occupied by moose, of genes in a small number of species, fare waged by white-tailed deer against the moose disappear. but their effects can be important and moose, mule deer, and pronghorn. As an example of extended pheno- widespread. White-tailed deer, Odocoileus virgini- types and community genetics, Whit- Many years ago, E. B. Ford published anus, are often infected by the ham and colleagues rely on their own an influential book entitled Ecological meningial worm, Parelaphostrongylus work on the ecology of the piñon– Genetics (1971). In those days, ecologi- tenuis. Deer become infected by acci- juniper woodland at Sunset Crater, dentally swallowing infected slugs or Arizona. Sunset Crater erupted approx- cal genetics was the study of genetic re- snails as they browse on shrubs and imately 800 years ago, depositing a deep sponses to environmental variability. grasses. The worms are released from layer of pea-sized lava pebbles that have Community genetics is a new form of the slug or snail as it is digested, but the low levels of nutrients and do not retain ecological genetics, in which the genes worm evades digestion by burrowing water as well as normal soils. In this not only respond to the environment out of the deer’s digestive system. stressful environment, the stem-boring but also change physical and biotic Worms travel along the spinal cord to moth, Dioryctria albovittella, rises to components of the environment. Com- the meninges, the soft tissues that cush- epidemic levels, profoundly affecting munity genetics may truly merge the ion the brain. Here they lay eggs that are the piñon, Pinus edulis. Approximately fields of ecology and evolution. then transported by the circulatory sys- 20 percent of these trees are resistant to tem to the lungs. The deer coughs up the moths, but the susceptible trees suf- References cited the parasites, swallows them, and then fer such severe, chronic herbivory that Combes C. 2001. Parasitism: The Ecology and passes them in its feces. The life cycle of their growth form is modified to that of Evolution of Intimate Interactions. Chicago: the meningial worm is completed when a shrub and their production of female University of Chicago Press. the worms are acquired by a slug or cones is all but eliminated. Electro- Dawkins R. 1982. The Extended Phenotype: The snail attracted to the feces. The majority phoretic studies have revealed a genetic Gene as the Unit of Selection. Oxford (United of infected white-tailed deer are asymp- component to resistance. This gives rise Kingdom): Oxford University Press. tomatic, but the infection runs a very to a mosaic of susceptible and resistant Ford EB. 1971. Ecological Genetics. London: different course in mule deer, prong- trees, with impacts on birds, seed- Chapman and Hall. horn antelope, bighorn sheep, and eating mammals, and the community Goodnight CJ. 1990. Experimental studies of moose. These species, like white-tailed of 600 microbial species associated with community evolution, I: The response to deer, acquire meningial worms by acci- piñon roots, including ectomycorrhizal selection at the community level. Evolution dentally eating infected slugs and snails. fungi. 44: 1614–1624. But in these other species, the worms Whitham and colleagues predict that Whitham TG, et al. 2003. Community and ecosystem genetics: A consequence of the first migrate to the meninges, then dominant species and keystone species extended phenotype. Ecology 84: 559–573. move into the brain. The infections will be most likely to support commu- cause severe neurologic disease leading nity genetics, and that within these Jeffry B. Mitton teaches in the Department of to paralysis and death. Tolerance of the species, only genes with major effects Ecology and Evolution at the University of meningial worm has consequences for will have the appropriate extended Colorado, Boulder, CO 80309. March 2003 / Vol. 53 No. 3 • BioScience 209.
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