Environmental Effects on the Expression of Life Span and Aging
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University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Faculty Publications in the Biological Sciences Papers in the Biological Sciences 9-2008 Environmental Effects on the Expression of Life Span and Aging: An Extreme Contrast between Wild and Captive Cohorts of Telostylinus angusticollis (Diptera: Neriidae) Noriyoshi Kawasaki Evolution and Ecology Research Centre and School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney 2052, New South Wales, Australia Chad Brassil University of Nebraska - Lincoln, [email protected] Robert Brooks Evolution and Ecology Research Centre and School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney 2052, New South Wales, Australia Russell Bonduriansky Evolution and Ecology Research Centre and School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney 2052, New South Wales, Australia Follow this and additional works at: https://digitalcommons.unl.edu/bioscifacpub Part of the Life Sciences Commons Kawasaki, Noriyoshi; Brassil, Chad; Brooks, Robert; and Bonduriansky, Russell, "Environmental Effects on the Expression of Life Span and Aging: An Extreme Contrast between Wild and Captive Cohorts of Telostylinus angusticollis (Diptera: Neriidae)" (2008). Faculty Publications in the Biological Sciences. 7. https://digitalcommons.unl.edu/bioscifacpub/7 This Article is brought to you for free and open access by the Papers in the Biological Sciences at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications in the Biological Sciences by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. vol. 172, no. 3 the american naturalist september 2008 Environmental Effects on the Expression of Life Span and Aging: An Extreme Contrast between Wild and Captive Cohorts of Telostylinus angusticollis (Diptera: Neriidae) Noriyoshi Kawasaki,1 Chad E. Brassil,2 Robert C. Brooks,1 and Russell Bonduriansky1,* 1. Evolution and Ecology Research Centre and School of From the standpoint of evolutionary biology an animal’s ex- Biological, Earth and Environmental Sciences, University of New pectation of life in its natural surroundings is much more South Wales, Sydney 2052, New South Wales, Australia; significant than the degree of decrepitude to which it may be 2. School of Biological Sciences, University of Nebraska, Lincoln, nursed in laboratory or zoo. (P. B. Medawar 1946) Nebraska 68588 Empirical research on life span and aging has largely relied Submitted October 24, 2007; Accepted February 28, 2008; Electronically published August 1, 2008 on captive populations of short-lived animals like Dro- sophila melanogaster, Caenorhabditis elegans, and mice (see Rose and Charlesworth 1981; Partridge and Barton 1993a, 1993b; Charlesworth and Hughes 1996; Jucker and Ingram 1997; Partridge and Mangel 1999; Kirkwood and Austad abstract: Most research on life span and aging has been based on 2000; Hughes et al. 2002). In contrast, we know remark- captive populations of short-lived animals; however, we know very ably little about life span and aging of short-lived organ- little about the expression of these traits in wild populations of such isms in their natural environments (see Medawar 1946; organisms. Because life span and aging are major components of fitness, the extent to which the results of many evolutionary studies Partridge 1988; Williams et al. 2006). This gap in knowl- in the laboratory can be generalized to natural settings depends on edge is especially problematic because the interpretation the degree to which the expression of life span and aging differ in of a wide range of evolutionary studies often rests on the natural environments versus laboratory environments and whether assumption that laboratory results are at least qualitatively such environmental effects interact with phenotypic variation. We informative of patterns that occur in wild populations, investigated life span and aging in Telostylinus angusticollis in the wild where the traits of interest evolved (Harshman and Hoff- while simultaneously estimating these parameters under a range of mann 2000). Because life span and aging (i.e., the pattern conditions in a laboratory stock that was recently established from the same wild population. We found that males live less than one- of age-related changes in the probability of survival and fifth as long and age at least twice as rapidly in the wild as do their reproduction) are major components of fitness, the as- captive counterparts. In contrast, we found no evidence of aging in sumption that laboratory results can be generalized to nat- wild females. These striking sex-specific differences between captive ural environments may be violated if life span and aging and wild flies support the emerging view that environment exerts a differ substantially between natural settings and laboratory profound influence on the expression of life span and aging. These settings. In particular, if environmental effects on the ex- findings have important implications for evolutionary gerontology pression of life span and aging interact with phenotypic and, more generally, for the interpretation of fitness estimates in variation (e.g., sex, age cohort, genetic or conditional captive populations. morph, etc.), then exposure to laboratory environments may yield patterns that are qualitatively different from Keywords: aging, senescence, environment, natural population, field those occurring in natural environments. Here we provide study, phenotypic plasticity, Telostylinus angusticollis. evidence of large, sex-dependent differences in life span and aging between cohorts observed in fully natural en- vironments versus genetically similar cohorts observed in laboratory environments. We argue that such effects may * Corresponding author; e-mail: [email protected]. complicate the interpretation of many laboratory studies Am. Nat. 2008. Vol. 172, pp. 346–357. ᭧ 2008 by The University of Chicago. and highlight the need for a better understanding of en- 0003-0147/2008/17203-50003$15.00. All rights reserved. vironmental effects on the expression of life span and DOI: 10.1086/589519 aging. Environment, Life Span, and Aging 347 Currently available evidence yields contradictory clues through the choice of model species with a sufficient site about how wild and captive populations differ in aging fidelity to yield reasonably high individual resighting rates, rates and life spans. For example, in wild rodents it re- such as insects that form stable mating aggregations (see mains unclear whether aging occurs at all (Slade 1995), Bonduriansky and Brassil 2002, 2005). whereas Bonduriansky and Brassil (2002) observed rapid We employed a mark-release-resight method to inves- aging in wild antler flies. Curiously, recent studies based tigate life span and actuarial aging (i.e., a change in mor- on common-garden assays have suggested that wild D. tality rate with age, henceforth “aging”) in the wild in melanogaster and mice have the genetic potential to age Telostylinus angusticollis (Neriidae), a large fly that forms more slowly and to live longer than their laboratory- mating aggregations on damaged tree trunks (Bondurian- adapted counterparts (Sgro` and Partridge 2000; Linnen et sky 2006, 2007; fig. 1). At the same time, we estimated al. 2001; Miller et al. 2002). However, in relation to the life span and aging under a variety of conditions (e.g., question of how wild organisms and captive organisms individual housing vs. grouped housing, same-sex groups differ in life span and rate of aging, the relevance of these vs. mixed-sex groups) in a laboratory stock that was re- common-garden studies is unclear because aging and life cently established from the same wild source population. span are highly plastic traits. The radically different en- We also experimentally tested for effects on mortality of vironments experienced by wild organisms and captive our marking technique as a result of mechanical injury or organisms could have large effects on the expression of paint toxicity. Modeling of mortality rate as a function of these traits, and such effects could either negate or amplify age using maximum likelihood techniques revealed a strik- any genetic differences between wild and laboratory- ing contrast between wild and captive flies in life span, adapted populations. Genotype # environment interac- rate of aging, and effects of sex. tions for life span have been observed in D. melanogaster (Vieira et al. 2000; Marden et al. 2003) and C. elegans (Shook and Johnson 1999; Van Voorhies et al. 2005). Life Methods span and aging rate are affected by diet in many animals Study Animals (Medawar 1946; Nishiyama et al. 1997; Masoro 2005); even the scent of food affects life span in Drosophila (Libert We studied a wild population of Telostylinus angusticollis et al. 2007). In rats, an enriched environment reduces the (Enderlein) in the Fred Hollows Reserve, Sydney, Austra- rate of brain aging (Saito et al. 1994; Nakamura et al. lia. The flies formed mixed-sex aggregations on two beetle- 1999). In ungulates, aging rate in wild males appears to damaged Acacia longifolia trees and could be found spo- be affected by population density (Mysterud et al. 2001). radically on several other trees and a wooden fence nearby. Consequently, comparisons of wild and captive popula- Telostylinus angusticollis adults fed, mated, and oviposited tions must take into account