Evolutionary Ecology, Antibiosis, and All That Rot

COMMENTARY Evolutionary ecology, antibiosis, and all that rot Michael Kasparia,1 and Bradley Stevensonb Graduate Program in Ecology and Evolutionary Biology, Departments of aZoology and bBotany and Microbiology, University of Oklahoma, Norman, OK 73019 ity members of the Animal Kingdom. They must compete for prey that hide, defend them- selves, or run away. This compe- Ptition only intensifies when such prey die uneaten. The carcasses and leaves strewn across the landscape are now available to microbial competitors that are everywhere, grow rapidly, and know how to poison. So how can an animal scavenger make a living? In a study in this issue of PNAS (1) Nicrophorus beetles that raise their grubs on mouse carcasses are shown to use a 2-pronged strategy: avoid the nastiest carcasses and apply the antibiotics. Ecologists have typically studied competition among suites of closely related species (e.g., 5 species of Dendroica warblers) (2). However, in 1977, evolutionary ecologist Dan Janzen (3) pointed out that a large fraction of potential food—fruits, seeds, and carcasses—may be lost to animals through competition with bacteria and fungi. Microbes have a Fig. 1. Most animals do not eat carcasses because microbes get there first, spreading rapidly and huge advantage, after all, because they poisoning the food with antibiotics (blue dots). Burying beetles fight back by regurgitating antibiotics (pink puddles) that lyse bacteria and preserve the carcass for their larvae. Illustration by Deborah Kaspari. are abundant both in the soil and the gut of the carcass. In warm environ- ments, they can also reproductively at maturity of the larval offspring, tious diseases, we know surprisingly lit- overrun a carcass before it can be dis- something often lacking in studies of tle about its evolutionary ecology. Most covered by a hungry animal. Janzen competition. They found that female ecologists study macrobes and have deposited that the resulting malodorous Nicrophorus preferred to raise young on voted little attention to antibiosis, a hydrogen sulfide and fatty acids that say freshly thawed mouse carcasses com- form of interference competition—the ‘‘rotten’’ in any language may in fact be pared with those that sat at room tem- allocation of resources, not to grow microbial messages proclaiming ‘‘this perature for 7 days (with the expected yourself, but to suppress the growth of food is taken.’’ Few options were con- olfactory result). Furthermore, larvae sidered open to scavengers, other than your competitors. Early models found it grown on rotten carcasses were 10% to specialize on efficient discovery (i.e., hard to conjure scenarios in which an smaller (size is a good predictor of fu- be a vulture) or only eat a carcass when animal engaging in costly, spiteful be- ture reproductive success in insects). it is ‘‘still warm’’(i.e., be an opportunist) havior could invade a new community (4). In this view, spoilage, not ingestion, Moreover, if stuck with a rotten carcass, (8, 9). As it turns out, the secret to suc- should be the common fate of the dead. the mothers could still do something cessful antibiosis is staying put. When Some animals, it turns out, may have about it. Before their eggs hatched, you give antibiotic-producing bacteria a additional options. Rozen and col- mothers deposited anal and oral secre- structured medium, they affix to sub- leagues (1), in a clever set of experi- tions. Brood on old carcasses who were strate, grow clonally, and produce a ‘‘no ments, suggest animals may also employ deprived of this prenatal care were mans land,’’ absent competitors, where antibiotics—small molecules like pep- smaller and took longer to develop than the antibiotics diffuse outward. Carrion tides, glycopeptides, terpenes, and alka- those raised on fresh carcasses. The au- and soil are full of such structure. Mov- loids that are effective at low densities thors conclude that there is something ing microbes out of the chemostat and in suppressing microbial competitors (5). in the parental care, especially those into a more structured, realistic world They studied the burying beetle, Nicro- secretions, which kept decomposer mi- [as Rozen and colleagues (1) do] has phorus vespilloides, which uses small crobes at bay [carcasses treated with been a dependable recipe for insight mammal carcasses as eat-in nurseries Nicrophorus secretions have been shown (Fig. 1). Nicrophorus parent their young to grow less fungi (6) and bacteria (7)]. and tend the carcass in which they bur- They acknowledge that how, exactly, the Author contributions: M.K. and B. S. wrote the paper. row. This was doubly fortuitous. First, microbes decrease the fitness of beetle The authors declare no conflict of interest. Rozen and colleagues had an animal larvae and what, precisely, is in the se- See companion article on page 17890 in issue 46 of volume that was heavily invested in keeping a cretions produced by the mothers, are 105. carcass’s microbe titer in check. Second, both open questions. 1To whom correspondence should be addressed. E-mail: the scientists could measure beetle fit- Despite the importance of under- [email protected]. ness: the survival, growth rate, and size standing antibiosis in a world of infec- © 2008 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0810507105 PNAS ͉ December 9, 2008 ͉ vol. 105 ͉ no. 49 ͉ 19027–19028 Downloaded by guest on September 29, 2021 into microbial evolutionary ecology soil fungi commingle when grown on like sowbugs and millipedes (isopods (10, 11). water, but generate ‘‘no man’s lands’’ and diplopods), have consortia of bacte- One surprising result of this study: when raised on richer malt agar (14). At ria and fungi in their guts (16); similar mother beetles raised their young on the high end, readily available sources of consortia in the foreguts of ruminants fresh carcasses, even as they preferred carbon, energy, nitrogen, and phosphate help detoxify plant secondary metabo- to consume ones that had been moul- can inhibit the production of a wide ar- lites (17). As when our mothers breast- dering for a week. One reason may be ray of antibiotics (15). Penicillium fungi, fed us, Nicrophorus mothers may very the way that different microbes, with well be inoculating their young with differing tactics, accumulate and replace competent gut flora. Furthermore, if it each other as the carcass decomposes. Carcasses treated with takes time to develop the consortia and Decomposers that arrive early often act enzymes necessary to thrive on a well- like fast-growing (and palatable) weeds Nicrophorus secretions decomposed carcass, then larvae may (12). As microbes accumulate, resource best be raised on fresh carrion. This is quality declines, and decomposer com- have been shown to especially so if developmental pathways petition heats up. There may be increas- are sensitive to various chemical insults ing selection for resource defense, with grow less fungi and (18). It is interesting, in this regard, that existing clones up-regulating antimicro- larvae feeding on old carcasses begged bial genes, or competitive replacement bacteria. more for food from their mother’s crop. favoring strains and species that consti- New chemical and computational tutively generate antibiotics. tools continue to bring the microbial Indeed, models of optimal interfer- which must be kept at intermediate lev- world into clearer focus. As they do so, ence already exist from the study of ani- els of glucose to maximize antibiotic ecologists are finding new ways that mi- mal territoriality (13). Here’s the trans- yield, behave like territorial honeycreep- crobes impact macrobial niches. Micro- lation. When resources are abundant (a ers that defend trees with intermediate biologists, in turn, should look to eco- fresh carcass), maximal uptake is numbers of flowers (13). Microbiologists logical theory, developed initially with achieved without the help of antibiotics; will find much inspiration in the litera- macrobes in mind, for insights into the when resources are scarce (nothing but ture of behavioral ecology, which repre- way microbes behave and microbial bones), basal requirements go unmet sents some of the biggest successes in communities are organized. With only a when antibiotics are built. Antibiosis evolutionary biology. handful of steps from gene 3 develop- should thus be the optimal behavior If antibiotic warfare increases over mental pathway 3 enzymes, antibiotics, somewhere in the middle of the re- the early life of the carcass, this may and structural products (i.e., the microbial source spectrum. In fact, antibiosis is shed light on the dietary divergence be- niche), the next model systems in evolu- rare on poor resources: the mycelia of tween mother and grub. Other animals, tionary ecology may well be microbial. 1. Rozen DE, Engelmoer DJP, Smiseth PT (2008) Antimicro- 7. Hoback WW, Bishop AA, Kroemer J, Scalzitti J, Shaffer 13. Carpenter FL, MacMillen RE (1976) Threshold model of bial strategies in burying beetles breeding on carrion. JJ (2004) Differences among antimicrobial properties feeding territoriality and test with a Hawaiian Honey- Proc Natl Acad Sci USA 165:17890–17895. of carrion beetle secretions reflect phylogeny and ecol- creeper. Science 194:639–642. 2. MacArthur RH (1958) Population ecology of some warblers ogy. J Chem Ecol 30:719–729. 14. Stahla PD, Christensen M (1992) In vitro mycelial inter- of northeastern coniferous forests. Ecology 39:599–619. 8. Chao L, Levin BR (1981) Structured habitats and the actions among members of a soil microfungal commu- 3. Janzen DH (1977) Why fruits rot, seeds mold, and meat evolution of anticompetitor toxins in bacteria. Proc nity. Soil Biol Biochem 24:309–316. spoils. Am Nat 111:691–713. Natl Acad Sci USA 78:6324–6328. 15. Rokem JS, Lantz AE, Nielsen J (2007) Systems biology of 9. Durrett R, Levin S (1997) Allelopathy in spatially distrib- antibiotic production by microorganisms.

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