Genetically based demographic reconstructions require careful consideration of generation time
2022; Elsevier BV; Volume: 32; Issue: 8 Linguagem: Inglês
10.1016/j.cub.2022.03.048
ISSN1879-0445
AutoresVictoria J. Bakker, Myra E. Finkelstein, Jesse G. Delia, Daniel F. Doak, Steve Kirkland,
Tópico(s)Animal Behavior and Reproduction
ResumoGeneration time (G), generally defined as the mean age at which individuals reproduce in a population, is a critical component of genetically based demographic reconstructions using coalescent models. In their recent study in Current Biology, Robinson et al.1Robinson J.A. Bowie R.C.K. Dudchenko O. Aiden E.L. Hendrickson S.L. Steiner C.C. Ryder O.A. Mindell D.P. Wall J.D. Genome-wide diversity in the California condor tracks its prehistoric abundance and decline.Curr. Biol. 2021; 31: 2939-2946.e5Abstract Full Text Full Text PDF PubMed Scopus (25) Google Scholar present such a reconstruction with implications for understanding historical population sizes of Andean condors (Vultur gryphus), California condors (Gymnogyps californianus) and turkey vultures (Cathartes aura). However, here we argue that incorrect generation time estimates call into question their finding that the now critically endangered California condor once outnumbered the turkey vulture — currently the most abundant and widespread vulture in the Americas. Robinson et al.1Robinson J.A. Bowie R.C.K. Dudchenko O. Aiden E.L. Hendrickson S.L. Steiner C.C. Ryder O.A. Mindell D.P. Wall J.D. Genome-wide diversity in the California condor tracks its prehistoric abundance and decline.Curr. Biol. 2021; 31: 2939-2946.e5Abstract Full Text Full Text PDF PubMed Scopus (25) Google Scholar use a G for condors of 10 years — less than half the true value, which we estimate to be ∼25 years (Table S1). This shorter generation time inflates their historical effective population size (Ne) estimates, and their use of the same G for species with different life histories makes their relative abundance comparisons flawed. Here, we re-evaluate the findings of Robinson et al.1Robinson J.A. Bowie R.C.K. Dudchenko O. Aiden E.L. Hendrickson S.L. Steiner C.C. Ryder O.A. Mindell D.P. Wall J.D. Genome-wide diversity in the California condor tracks its prehistoric abundance and decline.Curr. Biol. 2021; 31: 2939-2946.e5Abstract Full Text Full Text PDF PubMed Scopus (25) Google Scholar to highlight the importance of carefully estimating G in demographic reconstructions, especially for species of conservation concern. Genetically based demographic reconstructions use genetic diversity patterns in contemporary individuals, along with an estimated mutation rate, to infer past Ne over time2Mather N. Traves S.M. Ho S.Y.W. A practical introduction to sequentially Markovian coalescent methods for estimating demographic history from genomic data.Ecol. Evol. 2019; 10: 579-589Crossref PubMed Scopus (41) Google Scholar. Mutation rates for these reconstructions are frequently derived from sequence divergence and estimated divergence times among taxa, yielding mutations per year, which is then converted to a per-generation mutation rate. For a fixed per-year mutation rate, increasing G linearly decreases Ne estimates but does not affect the overall shape of estimated Ne trends2Mather N. Traves S.M. Ho S.Y.W. A practical introduction to sequentially Markovian coalescent methods for estimating demographic history from genomic data.Ecol. Evol. 2019; 10: 579-589Crossref PubMed Scopus (41) Google Scholar,3Nadachowska-Brzyska K. Li C. Smeds L. Zhang G. Ellegren H. Temporal dynamics of avian populations during Pleistocene revealed by whole-genome sequences.Curr. Biol. 2015; 25: 1375-1380Abstract Full Text Full Text PDF PubMed Scopus (161) Google Scholar. Therefore, misspecifications of G are especially problematic when comparing past population trajectories among species or when absolute historical Ne informs current conservation decisions. Despite its importance, G is often not carefully defined or estimated when used in genetically based demographic reconstructions. There are several ways to define G4Caswell H. Matrix Population Models: Construction, Analysis and Interpretation.Second Edition. Sinauer Associates, 2001Google Scholar,5IUCN StandardsPetitions CommitteeGuidelines for using the IUCN Red List categories and criteria.2019http://www.iucnredlist.org/documents/RedListGuidelines.pdfGoogle Scholar, the most common being the mean age of parents at reproduction. In demographic reconstructions, authors sometimes estimate G as the age at first breeding, F, or twice the age at first breeding (Supplemental information), but we cannot find any published work validating these rules of thumb, which are not robust across species with different maturation, reproductive senescence or mortality rates. G can only be equal to age at first breeding for semelparous species, and thus this approach is inappropriate for most vertebrates. For birds, the ratio of G to F ranges from 1.1 to 6.7 (X— = 2.5; Supplemental information) and for New World vultures (Cathartidae) from 1.7 to 5.3 (X— = 2.8)6Bird J.P. Martin R. Akçakaya H.R. Gilroy J. Burfield I.J. Garnett S.T. Symes A. Taylor J. Şekercioğlu Ç.H. Butchart S.H.M. Generation lengths of the world's birds and their implications for extinction risk.Conserv. Biol. 2020; 34: 1252-1261Crossref PubMed Scopus (112) Google Scholar. Direct estimates of G rely on age-specific reproduction and survival4Caswell H. Matrix Population Models: Construction, Analysis and Interpretation.Second Edition. Sinauer Associates, 2001Google Scholar, but G can be estimated with validated proxies using mean F and either adult mortality, M, or lifespan, L6Bird J.P. Martin R. Akçakaya H.R. Gilroy J. Burfield I.J. Garnett S.T. Symes A. Taylor J. Şekercioğlu Ç.H. Butchart S.H.M. Generation lengths of the world's birds and their implications for extinction risk.Conserv. Biol. 2020; 34: 1252-1261Crossref PubMed Scopus (112) Google Scholar. Although estimates of F, M and L are frequently unavailable, recently published analyses based on actual or model-derived estimates of these parameters report proxy-based G for all birds6Bird J.P. Martin R. Akçakaya H.R. Gilroy J. Burfield I.J. Garnett S.T. Symes A. Taylor J. Şekercioğlu Ç.H. Butchart S.H.M. Generation lengths of the world's birds and their implications for extinction risk.Conserv. Biol. 2020; 34: 1252-1261Crossref PubMed Scopus (112) Google Scholar and mammals7Pacifici M. Santini L. Di Marco M. Baisero D. Francucci L. Grottolo Marasini G. Visconti P. Rondinini C. Generation length for mammals.Nat. Conserv. 2013; 5: 89-94Crossref Scopus (175) Google Scholar. We note that these recent analyses rely on current demographic rates, in which survival, and thus G, is likely to be lower than it would be in the absence of anthropogenic threats. Robinson et al.1Robinson J.A. Bowie R.C.K. Dudchenko O. Aiden E.L. Hendrickson S.L. Steiner C.C. Ryder O.A. Mindell D.P. Wall J.D. Genome-wide diversity in the California condor tracks its prehistoric abundance and decline.Curr. Biol. 2021; 31: 2939-2946.e5Abstract Full Text Full Text PDF PubMed Scopus (25) Google Scholar apply the same G to three cathartid vultures — Andean condors, California condors and turkey vultures — highlighting results for a G of 10 years, but also reporting results for G of five and 15 years. All three G values are substantial underestimates for both condor species, while five years is even below their mean age of first breeding (F, Table 1). Using readily available demographic data and validated proxies, we estimate G at 25 and 26 years for California and Andean condors, respectively, and at seven years for turkey vultures (Table 1). Robinson et al.1Robinson J.A. Bowie R.C.K. Dudchenko O. Aiden E.L. Hendrickson S.L. Steiner C.C. Ryder O.A. Mindell D.P. Wall J.D. Genome-wide diversity in the California condor tracks its prehistoric abundance and decline.Curr. Biol. 2021; 31: 2939-2946.e5Abstract Full Text Full Text PDF PubMed Scopus (25) Google Scholar justify equal G, stating that even if G differs now, over evolutionary time it should be the same. However, the condor species diverged ∼7 to 14 MYA from a common ancestor with turkey vultures1Robinson J.A. Bowie R.C.K. Dudchenko O. Aiden E.L. Hendrickson S.L. Steiner C.C. Ryder O.A. Mindell D.P. Wall J.D. Genome-wide diversity in the California condor tracks its prehistoric abundance and decline.Curr. Biol. 2021; 31: 2939-2946.e5Abstract Full Text Full Text PDF PubMed Scopus (25) Google Scholar and almost certainly had demographic rates that precluded an equivalent G for the time interval of the reconstruction by Robinson et al.1Robinson J.A. Bowie R.C.K. Dudchenko O. Aiden E.L. Hendrickson S.L. Steiner C.C. Ryder O.A. Mindell D.P. Wall J.D. Genome-wide diversity in the California condor tracks its prehistoric abundance and decline.Curr. Biol. 2021; 31: 2939-2946.e5Abstract Full Text Full Text PDF PubMed Scopus (25) Google Scholar California and Andean condors inherently have extremely low reproductive and mortality rates and are among the largest and most long-lived birds, while turkey vultures weigh <25% of the condor species, have higher reproductive and mortality rates, and a markedly shorter lifespan (Table 1).Table 1Corrected estimates of generation time (G) and historical effective population size (Ne).SpeciesAge at first breeding, FaEstimated mean age of first breeding or age at which half the population has initiated breeding.Clutch sizeBreeding intervalAdult survival, SbReported contemporary adult survival rates. Survival rates in the absence of modern anthropogenic threats are likely higher.Life span, LcLife span, defined as maximum longevity, is unknown for all three species but estimated to be greater than or equal to the values given, based on limited records.Mass (kg)Current population size (1000s)GG sourceNe (1000s)10 KYA0.2–1 MYACalifornia condor, Gymnogyps californianus711–20.95608.50.510Robinson et al.1Robinson J.A. Bowie R.C.K. Dudchenko O. Aiden E.L. Hendrickson S.L. Steiner C.C. Ryder O.A. Mindell D.P. Wall J.D. Genome-wide diversity in the California condor tracks its prehistoric abundance and decline.Curr. Biol. 2021; 31: 2939-2946.e5Abstract Full Text Full Text PDF PubMed Scopus (25) Google Scholar0.535.025This studydMean of relative lifespan proxy and adult mortality proxy based on F, S, and L values reported in this table. Relative lifespan proxy defined as G = F + z(L – F). z scales reproductive lifespan (L – F) to account for reproductive senescence. z was set to 0.236 for turkey vultures and 0.317 for condors based on6. Adult mortality proxy defined as G = F – 1 + [1/(1 – S)]. See Table S1 for additional details and sources.0.214.0Andean condor, Vultur gryphus10eAge at first breeding for Andean condors is unknown, but captive birds have been reported to breed at age 8. Age at first breeding is unknown for turkey vultures, but breeding behavior has been observed in two-year olds.11.5–20.9460116.710Robinson et al.1Robinson J.A. Bowie R.C.K. Dudchenko O. Aiden E.L. Hendrickson S.L. Steiner C.C. Ryder O.A. Mindell D.P. Wall J.D. Genome-wide diversity in the California condor tracks its prehistoric abundance and decline.Curr. Biol. 2021; 31: 2939-2946.e5Abstract Full Text Full Text PDF PubMed Scopus (25) Google Scholar2.010.026This studydMean of relative lifespan proxy and adult mortality proxy based on F, S, and L values reported in this table. Relative lifespan proxy defined as G = F + z(L – F). z scales reproductive lifespan (L – F) to account for reproductive senescence. z was set to 0.236 for turkey vultures and 0.317 for condors based on6. Adult mortality proxy defined as G = F – 1 + [1/(1 – S)]. See Table S1 for additional details and sources.0.83.8Turkey vulture, Cathartes aura3eAge at first breeding for Andean condors is unknown, but captive birds have been reported to breed at age 8. Age at first breeding is unknown for turkey vultures, but breeding behavior has been observed in two-year olds.2 (range 1–3)10.791721300010Robinson et al.1Robinson J.A. Bowie R.C.K. Dudchenko O. Aiden E.L. Hendrickson S.L. Steiner C.C. Ryder O.A. Mindell D.P. Wall J.D. Genome-wide diversity in the California condor tracks its prehistoric abundance and decline.Curr. Biol. 2021; 31: 2939-2946.e5Abstract Full Text Full Text PDF PubMed Scopus (25) Google Scholar3.017.07This studydMean of relative lifespan proxy and adult mortality proxy based on F, S, and L values reported in this table. Relative lifespan proxy defined as G = F + z(L – F). z scales reproductive lifespan (L – F) to account for reproductive senescence. z was set to 0.236 for turkey vultures and 0.317 for condors based on6. Adult mortality proxy defined as G = F – 1 + [1/(1 – S)]. See Table S1 for additional details and sources.4.626.2Life history traits for three cathartid vultures highlighted in Robinson et al.1Robinson J.A. Bowie R.C.K. Dudchenko O. Aiden E.L. Hendrickson S.L. Steiner C.C. Ryder O.A. Mindell D.P. Wall J.D. Genome-wide diversity in the California condor tracks its prehistoric abundance and decline.Curr. Biol. 2021; 31: 2939-2946.e5Abstract Full Text Full Text PDF PubMed Scopus (25) Google Scholar and our corrected G and Ne estimates based on these traits. Ages and breeding intervals are given in years. See Table S1 for additional G estimates and expanded notes and references, including sources for demographic data.a Estimated mean age of first breeding or age at which half the population has initiated breeding.b Reported contemporary adult survival rates. Survival rates in the absence of modern anthropogenic threats are likely higher.c Life span, defined as maximum longevity, is unknown for all three species but estimated to be greater than or equal to the values given, based on limited records.d Mean of relative lifespan proxy and adult mortality proxy based on F, S, and L values reported in this table. Relative lifespan proxy defined as G = F + z(L – F). z scales reproductive lifespan (L – F) to account for reproductive senescence. z was set to 0.236 for turkey vultures and 0.317 for condors based on6Bird J.P. Martin R. Akçakaya H.R. Gilroy J. Burfield I.J. Garnett S.T. Symes A. Taylor J. Şekercioğlu Ç.H. Butchart S.H.M. Generation lengths of the world's birds and their implications for extinction risk.Conserv. Biol. 2020; 34: 1252-1261Crossref PubMed Scopus (112) Google Scholar. Adult mortality proxy defined as G = F – 1 + [1/(1 – S)]. See Table S1 for additional details and sources.e Age at first breeding for Andean condors is unknown, but captive birds have been reported to breed at age 8. Age at first breeding is unknown for turkey vultures, but breeding behavior has been observed in two-year olds. Open table in a new tab Life history traits for three cathartid vultures highlighted in Robinson et al.1Robinson J.A. Bowie R.C.K. Dudchenko O. Aiden E.L. Hendrickson S.L. Steiner C.C. Ryder O.A. Mindell D.P. Wall J.D. Genome-wide diversity in the California condor tracks its prehistoric abundance and decline.Curr. Biol. 2021; 31: 2939-2946.e5Abstract Full Text Full Text PDF PubMed Scopus (25) Google Scholar and our corrected G and Ne estimates based on these traits. Ages and breeding intervals are given in years. See Table S1 for additional G estimates and expanded notes and references, including sources for demographic data. Because the analyses of Robinson et al.1Robinson J.A. Bowie R.C.K. Dudchenko O. Aiden E.L. Hendrickson S.L. Steiner C.C. Ryder O.A. Mindell D.P. Wall J.D. Genome-wide diversity in the California condor tracks its prehistoric abundance and decline.Curr. Biol. 2021; 31: 2939-2946.e5Abstract Full Text Full Text PDF PubMed Scopus (25) Google Scholar are based on estimated per-year mutation rates, their estimated Ne values scale linearly with G2Mather N. Traves S.M. Ho S.Y.W. A practical introduction to sequentially Markovian coalescent methods for estimating demographic history from genomic data.Ecol. Evol. 2019; 10: 579-589Crossref PubMed Scopus (41) Google Scholar,3Nadachowska-Brzyska K. Li C. Smeds L. Zhang G. Ellegren H. Temporal dynamics of avian populations during Pleistocene revealed by whole-genome sequences.Curr. Biol. 2015; 25: 1375-1380Abstract Full Text Full Text PDF PubMed Scopus (161) Google Scholar. After rescaling with more plausible G values (Table 1), estimated California condor Ne never exceeds that of turkey vultures. Indeed, using our G values, the estimated turkey vulture Ne 10,000 years ago was 6 and 23 times higher than that of Andean and California condors, respectively, consistent with the turkey vulture's larger ancestral range and broader ecological niche. California condors have suffered a severe population and genetic bottleneck8D'Elia J. Haig S.M. Mullins T.D. Miller M.P. Ancient DNA reveals substantial genetic diversity in the California condor (Gymnogyps californianus) prior to a population bottleneck.Condor. 2016; 118: 703-714Crossref Scopus (17) Google Scholar, and population estimates prior to their declines are unavailable; therefore, estimating their historical Ne through demographic reconstructions may provide useful context when establishing conservation targets. Unfortunately, by assigning the same G to these three cathartids and implicitly assuming they have similar life histories, Robinson et al.1Robinson J.A. Bowie R.C.K. Dudchenko O. Aiden E.L. Hendrickson S.L. Steiner C.C. Ryder O.A. Mindell D.P. Wall J.D. Genome-wide diversity in the California condor tracks its prehistoric abundance and decline.Curr. Biol. 2021; 31: 2939-2946.e5Abstract Full Text Full Text PDF PubMed Scopus (25) Google Scholar erroneously concluded that California condors were more numerous than turkey vultures 0.2–1 million years ago, an ecological comparison that could sharply alter recovery goals. Our rescaling indicates that California condors were never more numerous than turkey vultures and their populations 10,000 years ago were likely <5% that of turkey vultures, and ∼25% that of Andean condors. The use of genetically based demographic reconstructions, such as the Markovian coalescent methods used by Robinson et al.1Robinson J.A. Bowie R.C.K. Dudchenko O. Aiden E.L. Hendrickson S.L. Steiner C.C. Ryder O.A. Mindell D.P. Wall J.D. Genome-wide diversity in the California condor tracks its prehistoric abundance and decline.Curr. Biol. 2021; 31: 2939-2946.e5Abstract Full Text Full Text PDF PubMed Scopus (25) Google Scholar, can be valuable for inferring population histories of endangered species but require numerous assumptions and parameter estimates that can directly and seriously influence results9Loog L. Sometimes hidden but always there: The assumptions underlying genetic inference of demographic histories.Philos. Trans. R. Soc. B Biol. Sci. 2021; 376: 20190719Crossref PubMed Scopus (5) Google Scholar. We focus here on G, yet cross-species comparisons must also carefully consider specification of a mutation rate and other assumptions of coalescent models that may be violated, potentially confounding the interpretations of historical Ne. We urge particular caution when applying these methods to species of conservation concern, where biased estimates could contribute to inefficient management or the establishment of unrealistic conservation goals. The findings and conclusions in this article are those of the authors and do not necessarily represent the views of the U.S. Fish and Wildlife Service. V.J.B., M.E.F., and S.K. conceived of the manuscript; V.J.B., M.E.F., J.D., D.F.D., and S.K. wrote the manuscript. The authors declare no competing interests. Download .pdf (.41 MB) Help with pdf files Document S1. One Figure and One Table Genome-wide diversity in the California condor tracks its prehistoric abundance and declineRobinson et al.Current BiologyMay 13, 2021In BriefRobinson et al. sequence and analyze the genome of the Critically Endangered California condor. Genome-wide diversity in the California condor reveals evidence of historically high abundance followed by long-term decline, plus signs of recent inbreeding in the wild. Andean condor and turkey vulture genomes also show evidence of historical declines. Full-Text PDF Open AccessResponse to Bakker et al.Robinson et al.Current BiologyApril 25, 2022In BriefRobinson and colleagues respond to the points raised about their paper by Bakker et al. Full-Text PDF Open Archive
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