Evidence for GC-biased gene conversion as a driver of between-lineage differences in avian base composition
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- 作者：Claudia C Weber (1)
Bastien Boussau (2)
Jonathan Romiguier (3)
Erich D Jarvis (4)
Hans Ellegren (1)
1. Department of Evolutionary Biology ; Evolutionary Biology Centre ; Uppsala University ; Norbyv盲gen 18D ; SE-752 36 ; Uppsala ; Sweden
2. Laboratoire de Biom茅trie et Biologie Evolutive ; Universit茅 de Lyon ; Universit茅 Lyon 1 ; CNRS ; UMR5558 ; Villeurbanne ; France
3. CNRS ; Universit茅 Montpellier 2 ; UMR 5554 ; ISEM ; Montpellier ; France
4. Department of Neurobiology ; Howard Hughes Medical Institute ; Duke University Medical Center ; Durham ; NC ; USA - 刊名：Genome Biology
- 出版年：2014
- 出版时间：December 2014
- 年：2014
- 卷：15
- 期：12
- 全文大小：1,797 KB
- 参考文献：1. Wilson Sayres, MA, Venditti, C, Pagel, M, Makova, KD (2011) Do variations in substitution rates and male mutation bias correlate with life-history traits? A study of 32 mammalian genomes. Evolution 65: pp. 2800-2815 1111/j.1558-5646.2011.01337.x" target="_blank" title="It opens in new window">CrossRef
2. Lartillot, N, Delsuc, F (2012) Joint reconstruction of divergence times and life-history evolution in placental mammals using a phylogenetic covariance model. Evolution 66: pp. 1773-1787 1111/j.1558-5646.2011.01558.x" target="_blank" title="It opens in new window">CrossRef
3. Thomas, JA, Welch, JJ, Lanfear, R, Bromham, L (2010) A generation time effect on the rate of molecular evolution in invertebrates. Mol Biol Evol 27: pp. 1173-1180 CrossRef
4. Bromham, L (2011) The genome as a life-history character: why rate of molecular evolution varies between mammal species. Philos Trans R Soc Lond B Biol Sci 366: pp. 2503-2513 11.0014" target="_blank" title="It opens in new window">CrossRef
5. Lanfear, R, Kokko, H, Eyre-Walker, A (2014) Population size and the rate of evolution. Trends Ecol Evol 29: pp. 33-41 CrossRef
6. Akashi, H, Osada, N, Ohta, T (2012) Weak selection and protein evolution. Genetics 192: pp. 15-31 112.140178" target="_blank" title="It opens in new window">CrossRef
7. Nabholz, B, Uwimana, N, Lartillot, N (2013) Reconstructing the phylogenetic history of long-term effective population size and life-history traits using patterns of amino acid replacement in mitochondrial genomes of mammals and birds. Genome Biol Evol 5: pp. 1273-1290 CrossRef
8. Mancera, E, Bourgon, R, Brozzi, A, Huber, W, Steinmetz, LM (2008) High-resolution mapping of meiotic crossovers and non-crossovers in yeast. Nature 454: pp. 479-485 CrossRef
9. Lesecque, Y, Mouchiroud, D, Duret, L (2013) GC-biased gene conversion in yeast Is specifically associated with crossovers: Molecular mechanisms and evolutionary significance. Mol Biol Evol 30: pp. 1409-1419 CrossRef
10. Galtier, N, Duret, L (2007) Adaptation or biased gene conversion? Extending the null hypothesis of molecular evolution. Trends Genet 23: pp. 273-277 11" target="_blank" title="It opens in new window">CrossRef
11. Galtier, N, Piganeau, G, Mouchiroud, D, Duret, L (2001) GC-content evolution in mammalian genomes: the biased gene conversion hypothesis. Genetics 159: pp. 907-911
12. Webster, MT, Hurst, LD (2012) Direct and indirect consequences of meiotic recombination: implications for genome evolution. Trends Genet 28: pp. 101-109 11.11.002" target="_blank" title="It opens in new window">CrossRef
13. Muyle, A, Serres-Giardi, L, Ressayre, A, Escobar, J, Gl茅min, S (2011) GC-biased gene conversion and selection affect GC content in the Oryza genus (rice). Mol Biol Evol 28: pp. 2695-2706 CrossRef
14. Duret, L, Arndt, PF (2008) The impact of recombination on nucleotide substitutions in the human genome. PLoS Genet 4: pp. e1000071 CrossRef
15. Duret, L, Galtier, N (2009) Biased gene conversion and the evolution of mammalian genomic landscapes. Annu Rev Genomics Hum Genet 10: pp. 285-311 1146/annurev-genom-082908-150001" target="_blank" title="It opens in new window">CrossRef
16. Pessia, E, Popa, A, Mousset, S, Rezvoy, C, Duret, L, Marais, GAB (2012) Evidence for widespread GC-biased gene conversion in eukaryotes. Genome Biol Evol 4: pp. 675-682 CrossRef
17. Birdsell, JA (2002) Integrating genomics, bioinformatics, and classical genetics to study the effects of recombination on genome evolution. Mol Biol Evol 19: pp. 1181-1197 CrossRef
18. Spencer, CCA, Deloukas, P, Hunt, S, Mullikin, J, Myers, S, Silverman, B, Donnelly, P, Bentley, D, McVean, G (2006) The influence of recombination on human genetic diversity. PLoS Genet 2: pp. e148 CrossRef
19. Backstr枚m, N, Forstmeier, W, Schielzeth, H, Mellenius, H, Nam, K, Bolund, E, Webster, MT, Ost, T, Schneider, M, Kempenaers, B, Ellegren, H (2010) The recombination landscape of the zebra finch Taeniopygia guttata genome. Genome Res 20: pp. 485-495 1101/gr.101410.109" target="_blank" title="It opens in new window">CrossRef
20. Groenen, MAM, Wahlberg, P, Foglio, M, Cheng, HH, Megens, H-j, Crooijmans, RPM, Besnier, F, Lathrop, M, Muir, WM, Wong, GK-S, Gut, I, Andersson, L (2009) A high-density SNP-based linkage map of the chicken genome reveals sequence features correlated with recombination rate. Genome Res 19: pp. 510-519 1101/gr.086538.108" target="_blank" title="It opens in new window">CrossRef
21. Romiguier, J, Ranwez, V, Douzery, EJP, Galtier, N (2010) Contrasting GC-content dynamics across 33 mammalian genomes: relationship with life-history traits and chromosome sizes. Genome Res 20: pp. 1001-1009 1101/gr.104372.109" target="_blank" title="It opens in new window">CrossRef
22. Gossmann, TI, Woolfit, M, Eyre-Walker, A (2011) Quantifying the variation in the effective population size within a genome. Genetics 189: pp. 1389-1402 111.132654" target="_blank" title="It opens in new window">CrossRef
23. Nagylaki, T (1983) Evolution of a finite population under gene conversion. Proc Natl Acad Sci U S A 80: pp. 6278-6281 CrossRef
24. Lartillot, N (2013) Phylogenetic patterns of GC-biased gene conversion in placental mammals and the evolutionary dynamics of recombination landscapes. Mol Biol Evol 30: pp. 489-502 CrossRef
25. Maio, N, Schl枚tterer, C, Kosiol, C (2013) Linking great Apes genome evolution across time scales using polymorphism-aware phylogenetic models. Mol Biol Evol 30: pp. 2249-2262 CrossRef
26. Auton, A, Fledel-Alon, A, Pfeifer, S, Venn, O, S茅gurel, L, Street, T, Leffler, EM, Bowden, R, Aneas, I, Broxholme, J, Humburg, P, Iqbal, Z, Lunter, G, Maller, J, Hernandez, RD, Melton, C, Venkat, A, Nobrega, MA, Bontrop, R, Myers, S, Donnelly, P, Przeworski, M, McVean, G (2012) A fine-scale chimpanzee genetic map from population sequencing. Science 336: pp. 193-198 1126/science.1216872" target="_blank" title="It opens in new window">CrossRef
27. Farr茅, M, Micheletti, D, Ruiz-Herrera, A (2013) Recombination rates and genomic shuffling in human and chimpanzee鈥揳 new twist in the chromosomal speciation theory. Mol Biol Evol 30: pp. 853-864 CrossRef
28. Cl茅ment, Y, Arndt, PF (2011) Substitution patterns are under different influences in primates and rodents. Genome Biol Evol 3: pp. 236-245 11" target="_blank" title="It opens in new window">CrossRef
29. Ellegren, H (2010) Evolutionary stasis: the stable chromosomes of birds. Trends Ecol Evol 25: pp. 283-291 CrossRef
30. Shetty, S, Griffin, DK, Graves, JA (1999) Comparative painting reveals strong chromosome homology over 80 million years of bird evolution. Chromosome Res 7: pp. 289-295 CrossRef
31. Derjusheva, S, Kurganova, A, Habermann, F, Gaginskaya, E (2004) High chromosome conservation detected by comparative chromosome painting in chicken, pigeon and passerine birds. Chromosome Res 12: pp. 715-723 CrossRef
32. Guttenbach, M, Nanda, I, Feichtinger, W, Masabanda, JS, Griffin, DK, Schmid, M (2003) Comparative chromosome painting of chicken autosomal paints 1鈥? in nine different bird species. Cytogenet Genome Res 103: pp. 173-184 1159/000076309" target="_blank" title="It opens in new window">CrossRef
33. Jarvis, ED, Mirarab, S, Aberer, AJ, Li, B, Houde, P, Li, C, Ho, SYW, Faircloth, BC, Nabholz, B, Howard, JT, Suh, A, Weber, CC, Fonseca, RR, Li, J, Zhang, F, Li, H, Zhou, L, Narula, N, Liu, L, Ganapathy, G, Boussau, B, Bayzid, MS, Zavidovych, V, Subramanian, S, Gabald贸n, T, Capella-Guti茅rrez, S, Huerta-Cepas, J, Rekepalli, B, Munch, K, Schierup, M (2014) Whole-genome analyses resolve early branches in the tree of life of modern birds. Science 346: pp. 1320-1331 1126/science.1253451" target="_blank" title="It opens in new window">CrossRef
34. Warren, WC, Clayton, DF, Ellegren, H, Arnold, AP, Hillier, LW, K眉nstner, A (2010) The genome of a songbird. Nature 464: pp. 757-762 CrossRef
35. Oliver, PL, Goodstadt, L, Bayes, JJ, Birtle, Z, Roach, KC, Phadnis, N, Beatson, S, Lunter, G, Malik, HS, Ponting, CP (2009) Accelerated evolution of the Prdm9 speciation gene across diverse metazoan taxa. PLoS Genet 5: pp. e1000753 CrossRef
36. Axelsson, E, Webster, MT, Ratnakumar, A, Ponting, CP, Lindblad-Toh, K (2012) Death of PRDM9 coincides with stabilization of the recombination landscape in the dog genome. Genome Res 22: pp. 51-63 1101/gr.124123.111" target="_blank" title="It opens in new window">CrossRef
37. Lesecque, Y, Gl茅min, S, Lartillot, N, Mouchiroud, D, Duret, L (2014) The Red Queen model of recombination hotspots evolution in the light of archaic and modern human genomes. PLoS Genet 10: pp. e1004790 CrossRef
38. Mugal, CF, Arndt, PF, Ellegren, H (2013) Twisted signatures of GC-biased gene conversion embedded in an evolutionary stable karyotype. Mol Biol Evol 30: pp. 1700-1712 CrossRef
39. Martini, E, Diaz, RL, Hunter, N, Keeney, S (2006) Crossover homeostasis in yeast meiosis. Cell 126: pp. 285-295 CrossRef
40. McQueen, HA, Siriaco, G, Bird, AP, Mcqueen, HA (1998) Chicken microchromosomes are hyperacetylated, early replicating, and gene rich. Genome Res 8: pp. 621-630
Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432: pp. 695-716 CrossRef
41. Axelsson, E, Webster, M, Smith, N, Burt, D, Ellegren, H (2005) Comparison of the chicken and turkey genomes reveals a higher rate of nucleotide divergence on microchromosomes than macrochromosomes. Genome Res 15: pp. 120-125 1101/gr.3021305" target="_blank" title="It opens in new window">CrossRef
42. Webster, MT, Axelsson, E, Ellegren, H (2006) Strong regional biases in nucleotide substitution in the chicken genome. Mol Biol Evol 23: pp. 1203-1216 CrossRef
43. Duret, L, Semon, M, Mouchiroud, D, Galtier, N (2002) Vanishing GC-rich isochores in mammalian genomes. Genetics 1847: pp. 1837-1847
44. Belle, EMS, Duret, L, Galtier, N, Eyre-Walker, A (2004) The decline of isochores in mammals: an assessment of the GC content variation along the mammalian phylogeny. J Mol Evol 58: pp. 653-660 CrossRef
45. Smith, NGC, Eyre-Walker, A (2002) The compositional evolution of the murid genome. J Mol Evol 55: pp. 197-201 CrossRef
46. Nabholz, B, K眉nstner, A, Wang, R, Jarvis, ED, Ellegren, H (2011) Dynamic evolution of base composition: causes and consequences in avian phylogenomics. Mol Biol Evol 28: pp. 2197-2210 CrossRef
47. Zhang, G, Li, C, Li, Q, Li, B, Larkin, DM, Lee, C, Storz, JF, Antunes, A, Greenwold, MJ, Meredith, RW, Odeen, A, Cui, J, Zhou, Q, Xu, L, Pan, H, Wang, Z, Jin, L, Zhang, P, Hu, H, Yang, W, Hu, J, Xiao, J, Yang, Z, Liu, Y, Xie, Q, Yu, H, Lian, J, Wen, P, Zhang, F, Li, H (2014) Comprehensive avian phylogenomic analyses reveal novel and fundamental insights on genomic and phenotypic complexities of bird evolution. Science 346: pp. 1311-1320 1126/science.1251385" target="_blank" title="It opens in new window">CrossRef
48. Reis, M, Wernisch, L (2009) Estimating translational selection in eukaryotic genomes. Mol Biol Evol 26: pp. 451-461 CrossRef
49. K眉nstner, A, Nabholz, B, Ellegren, H (2011) Significant selective constraint at 4-fold degenerate sites in the avian genome and its consequence for detection of positive selection. Genome Biol Evol 3: pp. 1381-1389 112" target="_blank" title="It opens in new window">CrossRef
50. Doherty, A, McInerney, JO (2013) Translational selection frequently overcomes genetic drift in shaping synonymous codon usage patterns in vertebrates. Mol Biol Evol 30: pp. 2263-2267 CrossRef
51. Urrutia, AO, Hurst, LD (2001) Codon usage bias covaries with expression breadth and the rate of synonymous evolution in humans, but this is not evidence for selection. Genetics 159: pp. 1191-1199
52. Plotkin, JB, Kudla, G (2011) Synonymous but not the same: the causes and consequences of codon bias. Nat Rev Genet 12: pp. 32-42 CrossRef
53. Chamary, J-V, Parmley, JL, Hurst, LD (2006) Hearing silence: non-neutral evolution at synonymous sites in mammals. Nat Rev Genet 7: pp. 98-108 CrossRef
54. Piganeau, G, Mouchiroud, D, Duret, L, Gautier, C (2002) Expected relationship between the silent substitution rate and the GC content: implications for the evolution of isochores. J Mol Evol 54: pp. 129-133 11-3" target="_blank" title="It opens in new window">CrossRef
55. Park, C, Chen, X, Yang, J-R, Zhang, J (2013) Differential requirements for mRNA folding partially explain why highly expressed proteins evolve slowly. Proc Natl Acad Sci U S A 110: pp. E678-E686 110" target="_blank" title="It opens in new window">CrossRef
56. Zur, H, Tuller, T (2012) Strong association between mRNA folding strength and protein abundance in S. cerevisiae. EMBO Rep 13: pp. 272-277 11.262" target="_blank" title="It opens in new window">CrossRef
57. Galtier, N, Duret, L, Gl茅min, S, Ranwez, V (2009) GC-biased gene conversion promotes the fixation of deleterious amino acid changes in primates. Trends Genet 25: pp. 1-5 11" target="_blank" title="It opens in new window">CrossRef
58. Warnecke, T, Weber, CC, Hurst, LD (2009) Why there is more to protein evolution than protein function: splicing, nucleosomes and dual-coding sequence. Biochem Soc Trans 37: pp. 756-761 CrossRef
59. Galtier, N, Gouy, M (1998) Inferring pattern and process: maximum-likelihood implementation of a nonhomogeneous model of DNA sequence evolution for phylogenetic analysis. Eevolution 15: pp. 871-879
60. Romiguier, J, Ranwez, V, Douzery, EJP, Galtier, N (2013) Genomic evidence for large, long-lived ancestors to placental mammals. Mol Biol Evol 30: pp. 5-13 11" target="_blank" title="It opens in new window">CrossRef
61. Nee, S, Read, A, Greenwood, J, Harvey, P (1991) The relationship between abundance and body size in British birds. Nature 351: pp. 312-313 CrossRef
62. Rosenberg, NA (2002) The probability of topological concordance of gene trees and species trees. Theor Popul Biol 61: pp. 225-247 CrossRef
63. Lartillot, N, Poujol, R (2011) A phylogenetic model for investigating correlated evolution of substitution rates and continuous phenotypic characters. Mol Biol Evol 28: pp. 729-744 CrossRef
64. Duret, L, Eyre-Walker, A, Galtier, N (2006) A new perspective on isochore evolution. Gene 385: pp. 71-74 CrossRef
65. Romiguier, J, Figuet, E, Galtier, N, Douzery, EJP, Boussau, B, Dutheil, JY, Ranwez, V (2012) Fast and robust characterization of time-heterogeneous sequence evolutionary processes using substitution mapping. PLoS One 7: pp. e33852 CrossRef
66. Warnecke, T, Batada, NN, Hurst, LD (2008) The impact of the nucleosome code on protein-coding sequence evolution in yeast. PLoS Genet 4: pp. e1000250 CrossRef
67. Haddrath, O, Baker, AJ (2012) Multiple nuclear genes and retroposons support vicariance and dispersal of the palaeognaths, and an Early Cretaceous origin of modern birds. Proc Biol Sci 279: pp. 4617-4625 CrossRef
68. Amit, M, Donyo, M, Hollander, D, Goren, A, Kim, E, Gelfman, S, Lev-Maor, G, Burstein, D, Schwartz, S, Postolsky, B, Pupko, T, Ast, G (2012) Differential GC content between exons and introns establishes distinct strategies of splice-site recognition. Cell Rep 1: pp. 543-556 CrossRef
69. Gelfman, S, Cohen, N, Yearim, A, Ast, G (2013) DNA-methylation effect on cotranscriptional splicing is dependent on GC architecture of the exon-intron structure. Genome Res 23: pp. 789-799 1101/gr.143503.112" target="_blank" title="It opens in new window">CrossRef
70. Duret, L, Hurst, LD (2001) The elevated GC content at exonic third sites is not evidence against neutralist models of isochore evolution. Mol Biol Evol 18: pp. 757-762 CrossRef
71. Nam, K, Ellegren, H (2012) Recombination drives vertebrate genome contraction. PLoS Genet 8: pp. e1002680 CrossRef
72. Johnson, KP (2004) Deletion bias in avian introns over evolutionary timescales. Mol Biol Evol 21: pp. 599-602 CrossRef
73. Webster, MT, Smith, NGC, Hultin-Rosenberg, L, Arndt, PF, Ellegren, H (2005) Male-driven biased gene conversion governs the evolution of base composition in human alu repeats. Mol Biol Evol 22: pp. 1468-1474 CrossRef
74. Dreszer, TR, Wall, GD, Haussler, D, Pollard, KS (2007) Biased clustered substitutions in the human genome: the footprints of male-driven biased gene conversion. Genome Res 17: pp. 1420-1430 1101/gr.6395807" target="_blank" title="It opens in new window">CrossRef
75. Berglund, J, Pollard, KS, Webster, MT (2009) Hotspots of biased nucleotide substitutions in human genes. PLoS Biol 7: pp. e26 CrossRef
76. Pink, CJ, Hurst, LD (2011) Late replicating domains are highly recombining in females but have low male recombination rates: implications for isochore evolution. PLoS One 6: pp. e24480 CrossRef
77. Popa, A, Samollow, P, Gautier, C, Mouchiroud, D (2012) The sex-specific impact of meiotic recombination on nucleotide composition. Genome Biol Evol 4: pp. 412-422 CrossRef
78. Gl茅min, S (2011) Surprising fitness consequences of GC-biased gene conversion. II Heterosis. Genetics 187: pp. 217-227 110.120808" target="_blank" title="It opens in new window">CrossRef
79. Smith, JJ, Kuraku, S, Holt, C, Sauka-Spengler, T, Jiang, N, Campbell, MS, Yandell, MD, Manousaki, T, Meyer, A, Bloom, OE, Morgan, JR, Buxbaum, JD, Sachidanandam, R, Sims, C, Garruss, AS, Cook, M, Krumlauf, R, Wiedemann, LM, Sower, SA, Decatur, WA, Hall, JA, Amemiya, CT, Saha, NR, Buckley, KM, Rast, JP, Das, S, Hirano, M, McCurley, N, Guo, P, Rohner, N (2013) Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution. Nat Genet 45: pp. 415-421 CrossRef
80. Romiguier, J, Ranwez, V, Delsuc, F, Galtier, N, Douzery, EJP (2013) Less is more in mammalian phylogenomics: AT-rich genes minimize tree conflicts and unravel the root of placental mammals. Mol Biol Evol 30: pp. 2134-2144 116" target="_blank" title="It opens in new window">CrossRef
81. Dunning, JBJ (2007) CRC Handbook of Avian Body Masses. CRC Press, Boca Raton, FL CrossRef
82. Magalh茫es, JP, Costa, J (2009) A database of vertebrate longevity records and their relation to other life-history traits. J Evol Biol 22: pp. 1770-1774 1111/j.1420-9101.2009.01783.x" target="_blank" title="It opens in new window">CrossRef
83. Weber, CC, Nabholz, B, Romiguier, J, Ellegren, H (2014) Kr/Kc but not dN/dS correlates positively with body mass in birds, raising implications for inferring lineage-specific selection. Genome Biol 15: pp. 542 1186/s13059-014-0542-8" target="_blank" title="It opens in new window">CrossRef
84. M酶ller, AP (2006) Sociality, age at first reproduction and senescence: comparative analyses of birds. J Evol Biol 19: pp. 682-689 1111/j.1420-9101.2005.01065.x" target="_blank" title="It opens in new window">CrossRef
85. Boussau, B, Sz枚llosi, GJ, Duret, L, Gouy, M, Tannier, E, Daubin, V (2013) Genome-scale coestimation of species and gene trees. Genome Res 23: pp. 323-330 1101/gr.141978.112" target="_blank" title="It opens in new window">CrossRef
86. Liu, L, Yu, L, Edwards, SV (2010) A maximum pseudo-likelihood approach for estimating species trees under the coalescent model. BMC Evol Biol 10: pp. 302 1186/1471-2148-10-302" target="_blank" title="It opens in new window">CrossRef
87. Zhang G, Li B, Li C, Gilbert MTP, Jarvis ED, The Avian Phylogenomics Consortium, Wang J: The avian phylogenomics project data. / GigaScience Database 2014, http://dx.doi.org/10.5524/101000 - 刊物主题：Animal Genetics and Genomics; Human Genetics; Plant Genetics & Genomics; Microbial Genetics and Genomics; Fungus Genetics; Bioinformatics;
- 出版者：BioMed Central
- ISSN：1465-6906
文摘
Background While effective population size (Ne) and life history traits such as generation time are known to impact substitution rates, their potential effects on base composition evolution are less well understood. GC content increases with decreasing body mass in mammals, consistent with recombination-associated GC biased gene conversion (gBGC) more strongly impacting these lineages. However, shifts in chromosomal architecture and recombination landscapes between species may complicate the interpretation of these results. In birds, interchromosomal rearrangements are rare and the recombination landscape is conserved, suggesting that this group is well suited to assess the impact of life history on base composition. Results Employing data from 45 newly and 3 previously sequenced avian genomes covering a broad range of taxa, we found that lineages with large populations and short generations exhibit higher GC content. The effect extends to both coding and non-coding sites, indicating that it is not due to selection on codon usage. Consistent with recombination driving base composition, GC content and heterogeneity were positively correlated with the rate of recombination. Moreover, we observed ongoing increases in GC in the majority of lineages. Conclusions Our results provide evidence that gBGC may drive patterns of nucleotide composition in avian genomes and are consistent with more effective gBGC in large populations and a greater number of meioses per unit time; that is, a shorter generation time. Thus, in accord with theoretical predictions, base composition evolution is substantially modulated by species life history.