title: Parallel evolution of senescence in annual fishes in response to extrinsic mortality.
abstract: BACKGROUND
  Early evolutionary theories of aging predict that populations which experience low extrinsic mortality evolve a retarded onset of senescence. Experimental support for this theory in vertebrates is scarce, in part for the difficulty of quantifying extrinsic mortality and its condition- and density-dependent components that -when considered- can lead to predictions markedly different to those of the "classical" theories. Here, we study annual fish of the genus Nothobranchius whose maximum lifespan is dictated by the duration of the water bodies they inhabit. Different populations of annual fish do not experience different strengths of extrinsic mortality throughout their life span, but are subject to differential timing (and predictability) of a sudden habitat cessation. In this respect, our study allows testing how aging evolves in natural environments when populations vary in the prospect of survival, but condition-dependent survival has a limited effect. We use 10 Nothobranchius populations from seasonal pools that differ in their duration to test how this parameter affects longevity and aging in two independent clades of these annual fishes.
  
  
  RESULTS
  We found that replicated populations from a dry region showed markedly shorter captive lifespan than populations from a humid region. Shorter lifespan correlated with accelerated accumulation of lipofuscin (an established age marker) in both clades. Analysis of wild individuals confirmed that fish from drier habitats accumulate lipofuscin faster also under natural conditions. This indicates faster physiological deterioration in shorter-lived populations.
  
  
  CONCLUSIONS
  Our data provide a strong quantitative example of how extrinsic mortality can shape evolution of senescence in a vertebrate clade. Nothobranchius is emerging as a genomic model species. The characterization of pairs of closely related species with different longevities should provide a powerful paradigm for the identification of genetic variations responsible for evolution of senescence in natural populations.
authors.affiliation: Fritz-Lipmann Institute for Age Research, Leibniz Institute, Jena, Germany.
authors.forename: Eva Terzibasi
authors.initials: ET
authors.lastname: Tozzini
authors.forename: Alexander
authors.initials: A
authors.lastname: Dorn
authors.forename: Enoch
authors.initials: E
authors.lastname: Ng'oma
authors.forename: Matej
authors.initials: M
authors.lastname: Polačik
authors.forename: Radim
authors.initials: R
authors.lastname: Blažek
authors.forename: Kathrin
authors.initials: K
authors.lastname: Reichwald
authors.forename: Andreas
authors.initials: A
authors.lastname: Petzold
authors.forename: Brian
authors.initials: B
authors.lastname: Watters
authors.forename: Martin
authors.initials: M
authors.lastname: Reichard
authors.forename: Alessandro
authors.initials: A
authors.lastname: Cellerino
mesh_terms: D000375:Aging; D000818:Animals; D002980:Climate; D017753:Ecosystem; D008062:Lipofuscin / Q000032:analysis; D008136:Longevity; D023701:Smegmamorpha / Q000145:classification* / Q000235:genetics* / Q000502:physiology
chemical_list: D008062:Lipofuscin
references.citation: Proc Biol Sci. 2005 Sep 22;272(1575):1941-7
references.pmid: 16191601
references.citation: PLoS One. 2008;3(12):e3866
references.pmid: 19052641
references.citation: J Gerontol A Biol Sci Med Sci. 1995 Nov;50(6):B327-36
references.pmid: 7583788
references.citation: Ageing Res Rev. 2013 Jan;12(1):214-25
references.pmid: 22884974
references.citation: Am Nat. 2010 Feb;175(2):147-59
references.pmid: 20050804
references.citation: FASEB J. 2011 Nov;25(11):3756-62
references.pmid: 22046003
references.citation: Gerontology. 1994;40(2-4):113-32
references.pmid: 7926851
references.citation: Age (Dordr). 2013 Apr;35(2):301-14
references.pmid: 22205409
references.citation: Nat Rev Genet. 2012 Jul 10;13(8):589-94
references.pmid: 22777128
references.citation: Genome Biol. 2009 Feb 11;10(2):R16
references.pmid: 19210790
references.citation: Curr Biol. 2007 Mar 6;17(5):452-4
references.pmid: 17306543
references.citation: J Theor Biol. 1966 Sep;12(1):12-45
references.pmid: 6015424
references.citation: PLoS Genet. 2008 Aug 15;4(8):e1000152
references.pmid: 18704191
references.citation: Exp Gerontol. 1983;18(1):29-38
references.pmid: 6347701
references.citation: Exp Gerontol. 2011 Apr;46(4):249-56
references.pmid: 21056099
references.citation: Mech Ageing Dev. 2005 Jun-Jul;126(6-7):794-803
references.pmid: 15888334
references.citation: Proc Biol Sci. 2004 Feb 7;271(1536):259-66
references.pmid: 15058436
references.citation: Science. 2009 Nov 13;326(5955):998-1001
references.pmid: 19797625
references.citation: Biogerontology. 2012 Oct;13(5):501-10
references.pmid: 22923174
references.citation: PLoS One. 2010 Oct 11;5(10):e13287
references.pmid: 20949019
references.citation: Science. 2010 Jan 15;327(5963):302-5
references.pmid: 20007865
references.citation: Curr Biol. 2010 May 11;20(9):R406-8
references.pmid: 20462482
references.citation: Evolution. 1993 Jun;47(3):877-887
references.pmid: 28567901
references.citation: Growth Dev Aging. 1999 Winter;63(4):151-70
references.pmid: 10892563
references.citation: Proc Biol Sci. 2003 Nov 7;270 Suppl 2:S189-91
references.pmid: 14667379
references.citation: Curr Biol. 2006 Feb 7;16(3):296-300
references.pmid: 16461283
references.citation: Aging Cell. 2012 Apr;11(2):252-61
references.pmid: 22221414
references.citation: PLoS One. 2011;6(8):e22684
references.pmid: 21850233
references.citation: Mol Phylogenet Evol. 2011 Dec;61(3):739-49
references.pmid: 21708276
references.citation: Mech Ageing Dev. 2012 May;133(5):226-33
references.pmid: 22487494
references.citation: Science. 2010 Apr 16;328(5976):321-6
references.pmid: 20395504
references.citation: Biol Bull. 2007 Aug;213(1):55-66
references.pmid: 17679720
references.citation: Aging Cell. 2009 Dec;8(6):726-37
references.pmid: 19780720
references.citation: PLoS Genet. 2009 Jan;5(1):e1000326
references.pmid: 19119422
references.citation: Nature. 2001 Dec 20-27;414(6866):901-5
references.pmid: 11780061
references.citation: Sci Aging Knowledge Environ. 2005 Feb 02;2005(5):re1
references.pmid: 15689603
references.citation: Science. 2005 Mar 25;307(5717):1928-33
references.pmid: 15790847
references.citation: Curr Biol. 2012 Nov 20;22(22):2140-3
references.pmid: 23084993
references.citation: Mech Ageing Dev. 2009 May;130(5):290-6
references.pmid: 19428446
references.citation: Genetics. 2009 Dec;183(4):1385-95
references.pmid: 19786620
references.citation: Proc Biol Sci. 2007 Apr 7;274(1612):943-50
references.pmid: 17251099
references.citation: J Fish Biol. 2011 Mar;78(3):796-809
references.pmid: 21366573
references.citation: Aging Cell. 2012 Apr;11(2):241-51
references.pmid: 22171971
references.citation: Age (Dordr). 2008 Sep;30(2-3):169-76
references.pmid: 19424866
references.citation: PLoS Biol. 2006 Jan;4(1):e7
references.pmid: 16363919
references.citation: Nat Genet. 2006 Jan;38(1):107-11
references.pmid: 16341223
references.citation: Exp Gerontol. 1979;14(3):149-55
references.pmid: 456446
references.citation: Nature. 2004 Oct 28;431(7012):1095-9
references.pmid: 15510147
references.citation: Trends Ecol Evol. 2006 Aug;21(8):458-63
references.pmid: 16766081
references.citation: Aging Cell. 2011 Oct;10(5):824-31
references.pmid: 21624037
references.citation: Aging Cell. 2005 Oct;4(5):223-33
references.pmid: 16164422
references.citation: Exp Gerontol. 2011 Dec;46(12):970-8
references.pmid: 21896325
references.citation: PLoS Genet. 2011 Sep;7(9):e1002306
references.pmid: 21980307
references.citation: Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3309-13
references.pmid: 10716732
references.citation: Aging Cell. 2006 Jun;5(3):275-8
references.pmid: 16842500