Higher resting metabolic rate in long-lived breeding Ansell's mole-rats (Fukomys anselli)
Status PubMed-not-MEDLINE Jazyk angličtina Země Velká Británie, Anglie Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
29018488
PubMed Central
PMC5610445
DOI
10.1186/s12983-017-0229-6
PII: 229
Knihovny.cz E-zdroje
- Klíčová slova
- Aging, Mole-rat, Oxidative stress, Reproduction, Resting metabolic rate,
- Publikační typ
- časopisecké články MeSH
BACKGROUND: Reproduction is an energetically expensive process that supposedly impairs somatic integrity in the long term, because resources are limited and have to be allocated between reproduction and somatic maintenance, as predicted by the life history trade-off model. The consequence of reduced investment in somatic maintenance is a gradual deterioration of function, i.e. senescence. However, this classical trade-off model gets challenged by an increasing number of contradicting studies. Here we report about an animal model, which adds more complexity to the ongoing debate. Ansell's mole-rats are long-lived social subterranean rodents with only the founder pair reproducing, while most of their offspring remain in the parental burrow system and do not breed. Despite of a clear reproductive trade-off, breeders live up to twice as long as non-breeders, a unique feature amongst mammals. METHODS: We investigated mass-specific resting metabolic rates (msRMR) of breeders and non-breeders to gain information about the physiological basis underlying the reproduction-associated longevity in Ansell's mole-rats. We assessed the thermoneutral zone (TNZ) for breeders and non-breeders separately by means of indirect calorimetry. We applied generalized linear mixed-effects models for repeated measurements using the msRMR in the respective TNZs. RESULTS: TNZ differed between reproductive and non-reproductive Ansell's mole-rats. Contrary to classical aging models, the shorter-lived non-breeders had significantly lower msRMR within the thermoneutral zone compared to breeders. CONCLUSION: This is the first study reporting a positive correlation between msRMR and lifespan based on reproductive status. Our finding contradicts common aging theories, but supports recently introduced models which do not necessarily link reproductive trade-offs to lifespan reduction.
Faculty of Biology University of Duisburg Essen Essen Germany
Faculty of Forestry and Wood Sciences Czech University of Life Sciences Praha Czech Republic
Faculty of Science University of South Bohemia České Budějovice Czech Republic
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Höhn A, Weber D, Jung T, Ott C, Hugo M, Kochlik B, Kehm R, Konig J, Grune T, Castro JP. Happily (n)ever after: aging in the context of oxidative stress, proteostasis loss and cellular senescence. Redox Biol. 2017;11:482–501. doi: 10.1016/j.redox.2016.12.001. PubMed DOI PMC
Kirkwood TBL, Holliday R. The evolution of ageing and longevity. Proc R Soc Lond B Biol Sci. 1979;205:531–546. doi: 10.1098/rspb.1979.0083. PubMed DOI
Deerenberg C, Pen I, Dijkstra C, Arkies B-J, Visser GH, Daan S. Parental energy expenditure in relation to manipulated brood size in the European kestrel Falco tinnunculus. ZACS. 1995;99:39–48.
McNab BK. The energetics of reproduction in endotherms and its implication for their conservation. Integr Comp Biol. 2006;46:1159–1168. doi: 10.1093/icb/icl016. PubMed DOI
Speakman JR. The physiological costs of reproduction in small mammals. Philos Trans R Soc Lond Ser B Biol Sci. 2008;363:375–398. doi: 10.1098/rstb.2007.2145. PubMed DOI PMC
Heldstab SA, van Schaik CP, Isler K. Getting fat or getting help? How female mammals cope with energetic constraints on reproduction. Front Zool. 2017;14:1–11. doi: 10.1186/s12983-017-0214-0. PubMed DOI PMC
Kirkwood TBL. Understanding ageing from an evolutionary perspective. J Intern Med. 2008;263:117–127. doi: 10.1111/j.1365-2796.2007.01901.x. PubMed DOI
Blount JD, Vitikainen EIK, Stott I, Cant MA. Oxidative shielding and the cost of reproduction. Biol Rev. 2016;91:483–497. doi: 10.1111/brv.12179. PubMed DOI
de Magalhaes JP, Costa J, Church GM. An analysis of the relationship between metabolism, developmental schedules, and longevity using phylogenetic independent contrasts. J Gerontol A Biol Sci Med Sci. 2007;62:149–160. doi: 10.1093/gerona/62.2.149. PubMed DOI PMC
Furness LJ, Speakman JR. Energetics and longevity in birds. Age. 2008;30:75–87. doi: 10.1007/s11357-008-9054-3. PubMed DOI PMC
Munshi-South J, Wilkinson GS. Bats and birds: exceptional longevity despite high metabolic rates. Ageing Res Rev. 2010;9:12–19. doi: 10.1016/j.arr.2009.07.006. PubMed DOI
Selman C, McLaren JS, Collins AR, Duthie GG, Speakman JR. The impact of experimentally elevated energy expenditure on oxidative stress and lifespan in the short-tailed field vole Microtus agrestis. Proc Biol Sci. 2008;275:1907–1916. doi: 10.1098/rspb.2008.0355. PubMed DOI PMC
Speakman JR, Talbot DA, Selman C, Snart S, McLaren JS, Redman P, Krol E, Jackson DM, Johnson MS, Brand MD. Uncoupled and surviving: individual mice with high metabolism have greater mitochondrial uncoupling and live longer. Aging Cell. 2004;3:87–95. doi: 10.1111/j.1474-9728.2004.00097.x. PubMed DOI
Speakman JR, Garratt M. Oxidative stress as a cost of reproduction: beyond the simplistic trade-off model. BioEssays. 2014;36:93–106. doi: 10.1002/bies.201300108. PubMed DOI
Speakman JR, Blount JD, Bronikowski AM, Buffenstein R, Isaksson C, Kirkwood TBL, Monaghan P, Ozanne SE, Beaulieu M, Briga M, et al. Oxidative stress and life histories: unresolved issues and current needs. Ecol Evol. 2015;5:5745–5757. doi: 10.1002/ece3.1790. PubMed DOI PMC
Burda H, Honeycutt RL, Begall S, Locker-Grütjen O, Scharff A. Are naked and common mole-rats eusocial and if so, why? Behav Ecol Sociobiol. 2000;47:293–303. doi: 10.1007/s002650050669. DOI
Bappert M-T, Burda H, Begall S. To mate or not to mate? Mate preference and fidelity in monogamous Ansell’s mole-rats, Fukomys anselli, Bathyergidae. Folia Zool. 2012;61:71–83.
Dammann P, Burda H. Sexual activity and reproduction delay ageing in a mammal. Curr Biol. 2006;16:R117–R118. doi: 10.1016/j.cub.2006.02.012. PubMed DOI
Burda H. Individual recognition and incest avoidance in eusocial common mole-rats rather than reproductive suppression by parents. Experientia. 1995;51:411–413. doi: 10.1007/BF01928906. PubMed DOI
Schielke CKM, Begall S, Burda H. Reproductive state does not influence activity budgets of eusocial Ansell’s mole-rats, Fukomys anselli (Rodentia, Bathyergidae): a study of locomotor activity by means of RFID. Mammal Biol. 2012;77:1–5. doi: 10.1016/j.mambio.2011.09.004. DOI
Skliba J, Lovy M, Hrouzkova E, Kott O, Okrouhlik J, Sumbera R. Social and environmental influences on daily activity pattern in free-living subterranean rodents: the case of a eusocial bathyergid. J Biol Rhythm. 2014;29:203–214. doi: 10.1177/0748730414526358. PubMed DOI
Henning Y, Vole C, Begall S, Bens M, Broecker-Preuss M, Sahm A, Szafranski K, Burda H, Dammann P. Unusual ratio between free thyroxine and free triiodothyronine in a long-lived mole-rat species with bimodal ageing. PLoS One. 2014;9:e113698. doi: 10.1371/journal.pone.0113698. PubMed DOI PMC
Begall S, Berendes M, Schielke CK, Henning Y, Laghanke M, Scharff A, van Daele P, Burda H. Temperature preferences of African mole-rats (family Bathyergidae) J Therm Biol. 2015;53:15–22. doi: 10.1016/j.jtherbio.2015.08.003. PubMed DOI
Lighton J. Measuring metabolic rates - a manual for scientists. New York: Oxford University Press; 2008.
Amaratunga D, Ge N. Step-down trend tests for identifying the minimum effective dose. J Biopharm Stat. 1998;8:151–162. doi: 10.1080/10543409808835228. PubMed DOI
Venkatraman E: clinfun: clinical trial design and data analysis functions. R package. R package version 1.0.10 edition; 2015.
Bates D, Machler M, Bolker B, Walker S: lme4: linear mixed-effects models using Eigen and S4. R package version 1.1–8 edition; 2015.
R Core Team . R: A language and environment for statistical computing. 2015.
Zelová J, Sumbera R, Sedlácek F, Burda H. Energetics in a solitary subterranean rodent, the silvery mole-rat, Heliophobius argenteocinereus, and allometry of RMR in African mole-rats (Bathyergidae) Comp Biochem Physiol A Mol Integr Physiol. 2007;147:412–419. doi: 10.1016/j.cbpa.2007.01.002. PubMed DOI
Douhard F, Lemaitre JF, Rauw WM, Friggens NC. Allometric scaling of the elevation of maternal energy intake during lactation. Front Zool. 2016;13:32. doi: 10.1186/s12983-016-0164-y. PubMed DOI PMC
Zheng G-X, Lin J-T, Zheng W-H, Cao J, Zhao Z-J. Energy intake, oxidative stress and antioxidant in mice during lactation. Zool Res. 2015;36:95–102. PubMed PMC
Schmidt CM, Jarvis JUM, Bennett NC. The long-lived queen: reproduction and longevity in female eusocial Damaraland mole-rats (Fukomys damarensis) Afr Zool. 2013;48:193–196. doi: 10.1080/15627020.2013.11407583. DOI
Scantlebury M, Speakman JR, Oosthuizen MK, Roper TJ, Bennett NC. Energetics reveals physiologically distinct castes in a eusocial mammal. Nature. 2006;440:795–797. doi: 10.1038/nature04578. PubMed DOI
Keil G, Cummings E, de Magalhães JP. Being cool: how body temperature influences ageing and longevity. Biogerontology. 2015;16:383–397. doi: 10.1007/s10522-015-9571-2. PubMed DOI PMC
Douhard F, Lemaître J-F, Rauw WM, Friggens NC: Allometric scaling of the elevation of maternal energy intake during lactation. Front Zool. 2016;13. doi:10.1186/s12983-016-0164-y. PubMed PMC
Yang DB, Xu YC, Wang DH, Speakman JR. Effects of reproduction on immuno-suppression and oxidative damage, and hence support or otherwise for their roles as mechanisms underpinning life history trade-offs, are tissue and assay dependent. J Exp Biol. 2013;216:4242–4250. doi: 10.1242/jeb.092049. PubMed DOI
Xu Y-C, Yang D-B, Speakman JR, Wang D-H. Oxidative stress in response to natural and experimentally elevated reproductive effort is tissue dependent. Funct Ecol. 2014;28:402–410. doi: 10.1111/1365-2435.12168. DOI
Vaanholt LM, Milne A, Zheng Y, Hambly C, Mitchell SE, Valencak TG, Allison DB, Speakman JR. Oxidative costs of reproduction: Oxidative stress in mice fed standard and low antioxidant diets. Physiol Behav. 2016;154:1–7. doi: 10.1016/j.physbeh.2015.11.009. PubMed DOI PMC
Sudyka J, Casasole G, Rutkowska J, Cichoń M. Elevated reproduction does not affect telomere dynamics and oxidative stress. Behav Ecol Sociobiol. 2016;70:2223–2233. doi: 10.1007/s00265-016-2226-8. PubMed DOI PMC
Oklejewicz M, Daan S. Enhanced longevity in tau mutant Syrian hamsters, Mesocricetus auratus. J Biol Rhythm. 2002;17:210–216. doi: 10.1177/07430402017003004. PubMed DOI
Echtay KS, Roussel D, St-Pierre J, Jekabsons MB, Cadenas S, Stuart JA, Harper JA, Roebuck SJ, Morrison A, Pickering S, et al. Superoxide activates mitochondrial uncoupling proteins. Nature. 2002;415:96–99. doi: 10.1038/415096a. PubMed DOI
Keipert S, Voigt A, Klaus S. Dietary effects on body composition, glucose metabolism, and longevity are modulated by skeletal muscle mitochondrial uncoupling in mice. Aging Cell. 2011;10:122–136. doi: 10.1111/j.1474-9726.2010.00648.x. PubMed DOI PMC
Salin K, Auer SK, Rudolf AM, Anderson GJ, Cairns AG, Mullen W, Hartley RC, Selman C, Metcalfe NB. Individuals with higher metabolic rates have lower levels of reactive oxygen species in vivo. Biol Lett. 2015;11:20150538. doi: 10.1098/rsbl.2015.0538. PubMed DOI PMC
Begall S, Burda H. Reproductive characteristics and growth in the eusocial Zambian Common mole-rat (Cryptomys sp., Bathyergidae) Mammal Biol - Z Säugetierkunde. 1998;63:297–306.
Burda H. Reproductive biology (behaviour, breeding, and postnatal development) in subterranean mole-rats, Cryptomys hottentotus (Bathyergidae) Mammal Biol - Z Säugetierkunde. 1989;54:360–376.
Brand MD. Uncoupling to survive? The role of mitochondrial inefficiency in ageing. Exp Gerontol. 2000;35:811–820. doi: 10.1016/S0531-5565(00)00135-2. PubMed DOI
Busiello RA, Savarese S, Lombardi A. Mitochondrial uncoupling proteins and energy metabolism. Front Physiol. 2015;6:36. doi: 10.3389/fphys.2015.00036. PubMed DOI PMC
Andziak B, O’Connor TP, Qi W, DeWaal EM, Pierce A, Chaudhuri AR, Van Remmen H, Buffenstein R. High oxidative damage levels in the longest-living rodent, the naked mole-rat. Aging Cell. 2006;5:463–471. doi: 10.1111/j.1474-9726.2006.00237.x. PubMed DOI
Detillion CE, Craft TKS, Glasper ER, Prendergast BJ, DeVries AC. Social facilitation of wound healing. Psychoneuroendocrinology. 2004;29:1004–1011. doi: 10.1016/j.psyneuen.2003.10.003. PubMed DOI