The evolution of prolonged life after reproduction
Authors: Darren P. Croft, Lauren J.N. Brent, Daniel W. Franks, Michael A. Cant
Journal: Trends in Ecology & Evolution (2015)

•The evolution of prolonged PRLSs is a scientific puzzle.•We discuss evidence for PRLSs in human and nonhuman animals.•We evaluate evidence for classic and modern hypotheses proposed to explain the evolution of PRLSs.•We argue that interacting mechanisms are needed to explain the evolution of PRLSs. Why females of some species cease ovulation before the end of their natural lifespan is a longstanding evolutionary puzzle. For many species in captivity, post-reproductive life is simply an epiphenomenon of lengthened lifespan. Yet in natural populations of humans as well as some cetaceans and insects, reproductive senescence occurs much faster than somatic aging and females exhibit prolonged post-reproductive lifespans (PRLSs). Determining the mechanisms and functions that underpin PRLSs has proved a significant challenge. Here we bring together both classic and modern hypotheses proposed to explain PRLSs and discuss their application to both human and nonhuman animals. By taking an integrative and broad taxonomic approach we highlight the need to consider multiple interacting explanations for the evolution of PRLSs. Why females of some species cease ovulation before the end of their natural lifespan is a longstanding evolutionary puzzle. For many species in captivity, post-reproductive life is simply an epiphenomenon of lengthened lifespan. Yet in natural populations of humans as well as some cetaceans and insects, reproductive senescence occurs much faster than somatic aging and females exhibit prolonged post-reproductive lifespans (PRLSs). Determining the mechanisms and functions that underpin PRLSs has proved a significant challenge. Here we bring together both classic and modern hypotheses proposed to explain PRLSs and discuss their application to both human and nonhuman animals. By taking an integrative and broad taxonomic approach we highlight the need to consider multiple interacting explanations for the evolution of PRLSs. Why females of some species cease ovulation before the end of their natural lifespan is a longstanding evolutionary puzzle [1Williams G.C. Pleiotropy, natural selection, and the evolution of senescence.Evolution. 1957; 11: 398-411Crossref Google Scholar, 2Hamilton W.D. The moulding of senescence by natural selection.J. Theor. Biol. 1966; 12: 12-45Crossref PubMed Scopus (1454) Google Scholar, 3Medawar P.B. An Unsolved Problem of Biology. H.K. Lewis, 1952Google Scholar]. Any decline in reproductive function is detrimental to Darwinian fitness and thus classical evolutionary theory predicts the early termination of reproduction should be selected against [2Hamilton W.D. The moulding of senescence by natural selection.J. Theor. Biol. 1966; 12: 12-45Crossref PubMed Scopus (1454) Google Scholar, 3Medawar P.B. An Unsolved Problem of Biology. H.K. Lewis, 1952Google Scholar]. Reproductive decline long before the end of life in humans has generated tremendous medical and evolutionary interest [1Williams G.C. Pleiotropy, natural selection, and the evolution of senescence.Evolution. 1957; 11: 398-411Crossref Google Scholar, 4Kirkwood T.B. Shanley D.P. The connections between general and reproductive senescence and the evolutionary basis of menopause.Ann. N. Y. Acad. Sci. 2010; 1204: 21-29Crossref PubMed Scopus (41) Google Scholar, 5Hawkes K. et al.Grandmothering, menopause, and the evolution of human life-histories.Proc. Natl. Acad. Sci. U.S.A. 1998; 95: 1336-1339Crossref PubMed Scopus (857) Google Scholar, 6Mace R. Evolutionary ecology of human life history.Anim. Behav. 2000; 59: 1-10Crossref PubMed Scopus (214) Google Scholar, 7Hill K. Hurtado A. The evolution of premature reproductive senescence and menopause in human females.Hum. Nat. 1991; 2: 313-350Crossref PubMed Scopus (147) Google Scholar, 8Austad S.N. Menopause: an evolutionary perspective.Exp. 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However, for several long-lived nonhuman mammals, detailed demographic data sets have matured sufficiently to allow life-history evolution to be studied in natural populations [14Lahdenperä M. et al.Reproductive cessation and post-reproductive lifespan in Asian elephants and pre-industrial humans.Front. Zool. 2014; 11: 54Crossref PubMed Scopus (66) Google Scholar, 22Ward E. et al.The role of menopause and reproductive senescence in a long-lived social mammal.Front. Zool. 2009; 6: 4Crossref PubMed Scopus (57) Google Scholar, 23Alberts S.C. et al.Reproductive aging patterns in primates reveal that humans are distinct.Proc. Natl. Acad. Sci. U.S.A. 2013; 110: 13440-13445Crossref PubMed Scopus (108) Google Scholar, 24Strier K.B. et al.The primate life history database: a unique shared ecological data resource.Methods Ecol. 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Why ageing occurs has been a central question in ecology and evolution for much of the past century [1Williams G.C. Pleiotropy, natural selection, and the evolution of senescence.Evolution. 1957; 11: 398-411Crossref Google Scholar, 2Hamilton W.D. The moulding of senescence by natural selection.J. Theor. Biol. 1966; 12: 12-45Crossref PubMed Scopus (1454) Google Scholar, 28Kirkwood T. Evolution of ageing.Nature. 1977; 270: 301-304Crossref PubMed Scopus (1354) Google Scholar, 29Kirkwood T.B. Austad S.N. Why do we age?.Nature. 2000; 408: 233-238Crossref PubMed Scopus (1271) Google Scholar]. There is general agreement that the evolution of senescence is unavoidably linked to the fact that under natural conditions organisms die from extrinsic hazards [29Kirkwood T.B. Austad S.N. Why do we age?.Nature. 2000; 408: 233-238Crossref PubMed Scopus (1271) Google Scholar, 30Promislow D.E. Senescence in natural populations of mammals: a comparative study.Evolution. 1991; 45: 1869-1887Crossref Google Scholar]. Since there are always fewer older individuals in a population than younger ones, the strength of selection on alleles with age-specific fitness effects is expected to weaken with increasing age [2Hamilton W.D. The moulding of senescence by natural selection.J. Theor. Biol. 1966; 12: 12-45Crossref PubMed Scopus (1454) Google Scholar, 3Medawar P.B. An Unsolved Problem of Biology. H.K. Lewis, 1952Google Scholar] and alleles that confer advantages early in life, by increasing early-life fecundity, can spread to fixation even if they have deleterious effects later [1Williams G.C. Pleiotropy, natural selection, and the evolution of senescence.Evolution. 1957; 11: 398-411Crossref Google Scholar, 31Charlesworth B. Evolution in Age-structured Populations. Cambridge University Press, 1994Crossref Google Scholar]. The declining strength of selection with age sets the stage for the evolution of physiological mechanisms leading to both reproductive and somatic senescence [28Kirkwood T. Evolution of ageing.Nature. 1977; 270: 301-304Crossref PubMed Scopus (1354) Google Scholar, 32Gavrilov L.A. Gavrilova N.S. The reliability theory of aging and longevity.J. Theor. Biol. 2001; 213: 527-545Crossref PubMed Scopus (337) Google Scholar]. Somatic and reproductive senescence are inherently linked: there is no benefit to an organism in maintaining a viable germline if somatic senescence has progressed to the point that prevents successful reproduction [4Kirkwood T.B. Shanley D.P. The connections between general and reproductive senescence and the evolutionary basis of menopause.Ann. N. Y. Acad. Sci. 2010; 1204: 21-29Crossref PubMed Scopus (41) Google Scholar]. Most vertebrate species typically show a gradual decline in reproduction with age [12Jones O.R. et al.Diversity of ageing across the tree of life.Nature. 2014; 505: 169-173Crossref PubMed Scopus (583) Google Scholar]. However, in some circumstances reproductive senescence is accelerated relative to somatic senescence leading to a PRLS. At first glance, PRLSs appear to be widespread and have been documented across a wide range of taxonomic groups [11Reznick D. et al.The evolution of senescence and post-reproductive lifespan in guppies (Poecilia reticulata).PLoS Biol. 2006; 4: 136-143Crossref Scopus (117) Google Scholar, 13Holmes D.J. Ottinger M.A. Birds as long-lived animal models for the study of aging.Exp. Gerontol. 2003; 38: 1365-1375Crossref PubMed Scopus (108) Google Scholar, 33Walker M.L. Herndon J.G. Menopause in nonhuman primates?.Biol. Reprod. 2008; 79: 398-406Crossref PubMed Scopus (133) Google Scholar, 34Ottinger M. Quail and other short-lived birds.Exp. Gerontol. 2001; 36: 859-868Crossref PubMed Scopus (52) Google Scholar] and in both males and females [35Vinicius L. et al.Variation in male reproductive longevity across traditional societies.PLoS ONE. 2014; 9: e112236Crossref PubMed Scopus (16) Google Scholar, 36Levitis D.A. et al.The human post-fertile lifespan in comparative evolutionary context.Evol. Anthropol. 2013; 22: 66-79Crossref PubMed Scopus (53) Google Scholar]. These patterns have led some authors to suggest that PRLSs are not an evolutionary oddity [9Cohen A.A. Female post-reproductive lifespan: a general mammalian trait.Biol. Rev. 2004; 79: 733-750Crossref PubMed Scopus (126) Google Scholar, 12Jones O.R. et al.Diversity of ageing across the tree of life.Nature. 2014; 505: 169-173Crossref PubMed Scopus (583) Google Scholar] and do not require special adaptive explanations [8Austad S.N. Menopause: an evolutionary perspective.Exp. Gerontol. 1994; 29: 255-263Crossref PubMed Scopus (73) Google Scholar, 37Finch C.E. Holmes D.J. Ovarian aging in developmental and evolutionary contexts.Ann. N. Y. Acad. Sci. 2010; 1204: 82-94Crossref PubMed Scopus (37) Google Scholar]. However, from an evolutionary perspective it is essential to consider both the context in which reproductive senescence occurs and how this trait is distributed within a population. Even if reproductive and somatic senescence generally occur at similar rates, variation in the relative timing of these processes will result in some individuals becoming post-reproductive before mortality [4Kirkwood T.B. Shanley D.P. The connections between general and reproductive senescence and the evolutionary basis of menopause.Ann. N. Y. Acad. Sci. 2010; 1204: 21-29Crossref PubMed Scopus (41) Google Scholar]. Many examples of PRLSs come from captive populations where individuals are released from extrinsic drivers of mortality (e.g., predators, disease) [8Austad S.N. Menopause: an evolutionary perspective.Exp. Gerontol. 1994; 29: 255-263Crossref PubMed Scopus (73) Google Scholar, 11Reznick D. et al.The evolution of senescence and post-reproductive lifespan in guppies (Poecilia reticulata).PLoS Biol. 2006; 4: 136-143Crossref Scopus (117) Google Scholar, 12Jones O.R. et al.Diversity of ageing across the tree of life.Nature. 2014; 505: 169-173Crossref PubMed Scopus (583) Google Scholar] or are subject to breeding programmes that can accelerate reproductive senescence [38Hermes R. et al.Reproductive problems directly attributable to long-term captivity-asymmetric reproductive aging.Anim. Reprod. Sci. 2004; 82–83: 49-60Abstract Full Text Full Text PDF PubMed Scopus (120) Google Scholar, 39Hermes R. et al.The effect of long non-reproductive periods on the genital health in captive female white rhinoceroses (Ceratotherium simum simum, C.s. cottoni).Theriogenology. 2006; 65: 1492-1515Abstract Full Text Full Text PDF PubMed Scopus (84) Google Scholar]. Thus PRLSs observed in captivity are most likely an artefact of delayed somatic senescence and/or accelerated reproductive senescence. Social and cultural factors can also result in a PRLS for some individuals. For example, PRLSs are common in men from some traditional societies [35Vinicius L. et al.Variation in male reproductive longevity across traditional societies.PLoS ONE. 2014; 9: e112236Crossref PubMed Scopus (16) Google Scholar]. However, unlike the women in these populations [36Levitis D.A. et al.The human post-fertile lifespan in comparative evolutionary context.Evol. Anthropol. 2013; 22: 66-79Crossref PubMed Scopus (53) Google Scholar], male PRLSs are the result of sociocultural constraints on opportunities for late-life reproduction rather than the physiological loss of fertility [40Bribiescas R.G. et al.Male life history, reproductive effort, and the evolution of the genus Homo: new directions and perspectives.Curr. Anthropol. 2012; 53: S424-S435Crossref Scopus (56) Google Scholar]. Such patterns are not driven by the decoupling of reproductive and somatic senescence and thus do not generate an evolutionary paradox. Here we focus our attention on PRLSs that are driven by the permanent cessation of fertility. What then is the evidence for PRLSs in nonhuman animals? Confusion has resulted from inconsistency in the definitions of menopause and PRLSs (Box 1). From an evolutionary perspective we want to know whether the rates of reproductive and somatic senescence have been decoupled in natural populations. We need to know not just whether post-reproductive females are observed in a population but also with what frequency and in what context they occur (Box 1). Recently, Levitis and Bingaman Lackey [41Levitis D.A. Bingaman Lackey L. A measure for describing and comparing postreproductive life span as a population trait.Methods Ecol. Evol. 2011; 2: 446-453Crossref PubMed Scopus (29) Google Scholar] proposed a new measure: post-reproductive representation (PrR) (Box 1) as a population measure of PRLS that allows comparisons across populations and species. We have collated female PrRs for published studies in Table 1. PrR is variable both within and among species and depends on population-specific mortality rates [41Levitis D.A. Bingaman Lackey L. A measure for describing and comparing postreproductive life span as a population trait.Methods Ecol. Evol. 2011; 2: 446-453Crossref PubMed Scopus (29) Google Scholar]. In humans, for example, PrR ranges from 0.31 in Trinidad plantation slaves to 0.76 in modern day Japan. In nonhuman primates, significant PrR values are observed only in captivity (Table 1), with healthy females living in the wild under natural mortality rates maintaining high birth rates late into life [26Thompson M.E. et al.Aging and fertility patterns in wild chimpanzees provide insights into the evolution of menopause.Curr. Biol. 2007; 17: 2150-2156Abstract Full Text Full Text PDF PubMed Scopus (186) Google Scholar, 42Wich S.A. et al.Life history of wild Sumatran orangutans (Pongo abelii).J. Hum. Evol. 2004; 47: 385-398Crossref PubMed Scopus (192) Google Scholar, 43Robbins A.M. et al.Age-related patterns of reproductive success among female mountain gorillas.Am. J. Phys. Anthropol. 2006; 131: 511-521Crossref PubMed Scopus (90) Google Scholar]. While elephants have a long lifespan, data on Asian elephants (Elephas maximus) suggest that reproductive function is maintained into late life in semi-natural populations [14Lahdenperä M. et al.Reproductive cessation and post-reproductive lifespan in Asian elephants and pre-industrial humans.Front. Zool. 2014; 11: 54Crossref PubMed Scopus (66) Google Scholar]. In insects, reproductive cessation has been reported in the gall-forming social aphid Quadrartus yoshinomiyai (Nipponaphidini), where post-reproductive females gain indirect fitness benefits through colony defence against predators (Figure 2) [18Uematsu K. et al.Juveniles and the elderly defend, the middle-aged escape: division of labour in a social aphid.Biol. Lett. 2013; 9: 20121053Crossref PubMed Scopus (14) Google Scholar, 19Uematsu K. et al.Altruistic colony defense by menopausal female insects.Curr. Biol. 2010; 20: 1182-1186Abstract Full Text Full Text PDF PubMed Scopus (43) Google Scholar]. Among vertebrates, humans, resident killer whales (Orcinus orca), and short-finned pilot whales (Globicephala macrorhynchus) are distinct in their patterns of reproductive and somatic senescence (Figure 1) and a significant proportion of females in populations of these species are post-reproductive (Table 1).Box 1Defining and measuring PRLSsThere are discrepancies in how the cessation of reproduction and PRLSs are defined, leading to confusion and misunderstandings. In humans reproductive cessation is generally defined operationally as the permanent cessation of menstruation (menopause) resulting from the loss of ovarian follicular activity [86Utian W.H. Menopause-related definitions.Int. Congr. Ser. 2004; 1266: 133-138Crossref Scopus (31) Google Scholar]. In nonhuman animals in the wild, determining ovulation cycles presents a significant challenge and reproductive cessation is often measured as the age at last birth [87Atsalis S. Videan E. Reproductive aging in captive and wild common chimpanzees: factors influencing the rate of follicular depletion.Am. J. Primatol. 2009; 71: 271-282Crossref PubMed Scopus (37) Google Scholar]. From an evolutionary perspective, it is the period of life after reproductive cessation that is of key interest. PRLSs are traditionally measured as the time between the end of fertility and the end of life (see [41Levitis D.A. Bingaman Lackey L. A measure for describing and comparing postreproductive life span as a population trait.Methods Ecol. Evol. 2011; 2: 446-453Crossref PubMed Scopus (29) Google Scholar] for a review) and is expressed as a population/species mean. Yet this measure is inherently biased because it includes only individuals that survive for a certain time after the last reproductive event and does not capture the importance of PRLSs for the population/species. This is elegantly illustrated in an example provided by Levitis et al. [36Levitis D.A. et al.The human post-fertile lifespan in comparative evolutionary context.Evol. Anthropol. 2013; 22: 66-79Crossref PubMed Scopus (53) Google Scholar]: in a semi-wild population of Macaca fuscata the mean PRLS measured at the end of fertility (22 years) is 3.1 years, suggesting that PRLS may be an important life-history period. However, fewer than 5% of adult females survive to a post-fertile age, clearly demonstrating that post-reproductive life is rare in this population. Moreover, measures of PRLS tend to be correlated with longevity, making comparisons across species problematic (Figure I). Recently a new measure – PrR [41Levitis D.A. Bingaman Lackey L. A measure for describing and comparing postreproductive life span as a population trait.Methods Ecol. Evol. 2011; 2: 446-453Crossref PubMed Scopus (29) Google Scholar] – has been proposed to quantify the significance of PRLSs and allow comparisons across populations/species. PrR is an unbiased population measure of reproductive lifespan. Under idealised demographic conditions, PrR equals the proportion of females that are post-reproductive. It is calculated from life tables using data from two ages: Age B – the beginning of adulthood, defined as the point at which 5% of lifetime fecundity has been realised, on average, independent of mortality; and Age M – the end of the fecund lifespan, defined as the point at which 95% of lifetime fecundity has been realised, on average, independent of mortality. PrR represents the number of years an average newborn can expect to live as a post-reproductive adult (beyond Age M) divided by the number of years an average newborn can expect to live as an adult (beyond Age B). Significance can be calculated using demographic simulations [41Levitis D.A. Bingaman Lackey L. A measure for describing and comparing postreproductive life span as a population trait.Methods Ecol. Evol. 2011; 2: 446-453Crossref PubMed Scopus (29) Google Scholar].Table 1Published values of female PrRr together with PrR for the resident killer whale calculated using published data 27Foster E.A. et al.Adaptive prolonged postreproductive life span in killer whales.Science. 2012; 337: 1313Crossref PubMed Scopus (122) Google Scholar (see Box 1 for a further description of PrR)SpeciesPopulationPrRRefs reporting PrRHumansHomo sapiensTrinidad plantation slaves 1783–18160.31536Levitis D.A. et al.The human post-fertile lifespan in comparative evolutionary context.Evol. Anthropol. 2013; 22: 66-79Crossref PubMed Scopus (53) Google ScholarH. sapiens!Kung0.42536Levitis D.A. et al.The human post-fertile lifespan in comparative evolutionary context.Evol. Anthropol. 2013; 22: 66-79Crossref PubMed Scopus (53) Google ScholarH. sapiensAche0.43936Levitis D.A. et al.The human post-fertile lifespan in comparative evolutionary context.Evol. Anthropol. 2013; 22: 66-79Crossref PubMed Scopus (53) Google ScholarH. sapiensHaiti 20020.46036Levitis D.A. et al.The human post-fertile lifespan in comparative evolutionary context.Evol. Anthropol. 2013; 22: 66-79Crossref PubMed Scopus (53) Google ScholarH. sapiensSweden 17510.47736Levitis D.A. et al.The human post-fertile lifespan in comparative evolutionary context.Evol. Anthropol. 2013; 22: 66-79Crossref PubMed Scopus (53) Google ScholarH. sapiensHadza0.48136Levitis D.A. et al.The human post-fertile lifespan in comparative evolutionary context.Evol. Anthropol. 2013; 22: 66-79Crossref PubMed Scopus (53) Google ScholarH. sapiensAfghanistan 20020.48636Levitis D.A. et al.The human post-fertile lifespan in comparative evolutionary context.Evol. Anthropol. 2013; 22: 66-79Crossref PubMed Scopus (53) Google ScholarH. sapiensPapua New Guinea 20020.48936Levitis D.A. et al.The human post-fertile lifespan in comparative evolutionary context.Evol. Anthropol. 2013; 22: 66-79Crossref PubMed Scopus (53) Google ScholarH. sapiensNiger 20020.49036Levitis D.A. et al.The human post-fertile lifespan in comparative evolutionary context.Evol. Anthropol. 2013; 22: 66-79Crossref PubMed Scopus (53) Google ScholarH. sapiensSomalia 20020.49736Levitis D.A. et al.The human post-fertile lifespan in comparative evolutionary context.Evol. Anthropol. 2013; 22: 66-79Crossref PubMed Scopus (53) Google ScholarH. sapiensPre-industrial Finns0.51214Lahdenperä M. et al.Reproductive cessation and post-reproductive lifespan in Asian elephants and pre-industrial humans.Front. Zool. 2014; 11: 54Crossref PubMed Scopus (66) Google ScholarH. sapiensUN Less Developed Regions 20020.60736Levitis D.A. et al.The human post-fertile lifespan in comparative evolutionary context.Evol. Anthropol. 2013; 22: 66-79Crossref PubMed Scopus (53) Google ScholarH. sapiensUN Less Developed Countries 20020.64336Levitis D.A. et al.The human post-fertile lifespan in comparative evolutionary context.Evol. Anthropol. 2013; 22: 66-79Crossref PubMed Scopus (53) Google ScholarH. sapiensUSA 20020.66836Levitis D.A. et al.The human post-fertile lifespan in comparative evolutionary context.Evol. Anthropol. 2013; 22: 66-79Crossref PubMed Scopus (53) Google ScholarH. sapiensSweden 20020.70736Levitis D.A. et al.The human post-fertile lifespan in comparative evolutionary context.Evol. Anthropol. 2013; 22: 66-79Crossref PubMed Scopus (53) Google ScholarH. sapiensJapan 20020.76036Levitis D.A. et al.The human post-fertile lifespan in comparative evolutionary context.Evol. Anthropol. 2013; 22: 66-79Crossref PubMed Scopus (53) Google ScholarNonhuman primatesBlue monkey (Cercopithecus mitis)Wild0.0223Alberts S.C. et al.Reproductive aging patterns in primates reveal that humans are distinct.Proc. Natl. Acad. Sci. U.S.A. 2013; 110: 13440-13445Crossref PubMed Scopus (108) Google ScholarBlue monkey (C. mitis)Wild0.04136Levitis D.A. et al.The human post-fertile lifespan in comparative evolutionary context.Evol. Anthropol. 2013; 22: 66-79Crossref PubMed Scopus (53) Google ScholarChimpanzee (Pan troglodytes)Wild0.01836Levitis D.A. et al.The human post-fertile lifespan in comparative evolutionary context.Evol. Anthropol. 2013; 22: 66-79Crossref PubMed Scopus (53) Google ScholarChimpanzee (P. troglodytes)Wild0.0223Alberts S.C. et al.Reproductive aging patterns in primates reveal that humans are distinct.Proc. Natl. Acad. Sci. U.S.A. 2013; 110: 13440-13445Crossref PubMed Scopus (108) Google ScholarChimpanzee (P. troglodytes)Zoo0.22436Levitis D.A. et al.The human post-fertile lifespan in comparative evolutionary context.Evol. Anthropol. 2013; 22: 66-79Crossref PubMed Scopus (53) Google ScholarGorilla (Gorilla beringei)Wild0.0423Alberts S.C. et al.Reproductive aging patterns in primates reveal that humans are distinct.Proc. Natl. Acad. Sci. U.S.A. 2013; 110: 13440-13445Crossref PubMed Scopus (108) Google ScholarHamadryas baboon (Papio hamadryas)Wild0.00536Levitis D.A. et al.The human post-fertile lifespan in comparative evolutionary context.Evol. Anthropol. 2013; 22: 66-79Crossref PubMed Scopus (53) Google ScholarHamadryas baboon (P. hamadryas)Zoo0.08436Levitis D.A. et al.The human post-fertile lifespan in comparative evolutionary context.Evol. Anthropol. 2013; 22: 66-79Crossref PubMed Scopus (53) Google ScholarJapanese macaque (Macaca fuscata)Semi-free ranging0.05436Levitis D.A. et al.The human post-fertile lifespan in comparative evolutionary context.Evol. Anthropol. 2013; 22: 66-79Crossr