Abstract
This paper investigates the complexity hypothesis in microbial evolutionary genetics from a philosophical vantage. This hypothesis, in its current version, states that genes with high connectivity (more functional connections to other genes) are likely to be resistant to being horizontally transferred. We defend four claims. (1) There is an important distinction between two different ways in which a gene family can persist: vertically and horizontally. There is a trade-off between these two modes of persistence, such that a gene better at achieving one will be worse at achieving the other. (2) At least some genes are likely to experience selection favoring increased transferability. One consequence of this can be encapsulated as the “simplicity hypothesis”: horizontally persisting genes will experience selection favoring reduced connectivity. (3) In order to make sense of the simplicity hypothesis, we need to consider evolutionary populations that transcend species boundaries. Vertical and horizontal persistence are therefore not two competing ways of succeeding at the same game, but involve playing two different games altogether. (4) The complexity hypothesis can be understood in terms of two related notions: entrenchment and Cuvierian functionalism. This framing reveals previously unrecognized and philosophically interesting connections between reasoning about deep conservation and horizontal transfer.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.Notes
We speak of gene family acquisition to distinguish this form of transfer from paralog addition, which also involves gene acquisition.
We raise this point because it constitutes a possible exception to the general existence of an inverse correlation between connectivity and transferability. An anonymous reviewer, however, suggests that this case might not be an exception: low but non-zero levels of coevolution could result in complex poisoning (the transferred protein interacts with the host complex, but dysfunctionally), and thus could render HGT deleterious. In the absence of empirical work, it is difficult to know how to balance these competing reasons.
In making this claim, we are considering only the effects of selection for transferability; other causes (as discussed in the “Vertical and Horizontal Persistence” section) might counteract these effects in real populations.
We are not positing selective processes that favor increased connectivity directly; it is enough for entrenchment to be a byproduct of selective processes. In Sober’s (1984) terms, what is required is selection of increased connectivity, not selection for it.
A quick note on terminology: throughout this section we will exclusively use “step” to refer to particular moves in the Cuvierian argument pattern, and “stage” to refer to temporal parts of organismal and evolutionary processes (e.g., developmental stages, stages of successful HGT).
Because of these features, Cuvierian functionalism can seem to suggest that species have fixed “types”, ignoring the variability of real populations. However, Cuvierian functionalism ultimately rests on a kind of selective process (filtering out of variants that disrupt integration), and thus requires variability. An explanation of stasis in terms of the absence of variants would not be Cuvierian functionalist. See Novick (2019) for a full discussion of these issues.
References
Ambler RP, Meyer TE, Kamen MD (1979) Anomalies in amino acid sequences of small cytochromes c and cytochromes c′ from two species of purple photosynthetic bacteria. Nature 278(5705):661–662. https://doi.org/10.1038/278661a0
Andam CP, Williams D, Gogarten JP (2010) Natural taxonomy in light of horizontal gene transfer. Biol Philos 25(4):589–602. https://doi.org/10.1007/s10539-010-9212-8
Appel TA (1987) The Cuvier-Geoffrey debate: French biology in the decades before Darwin. Oxford University Press, Oxford
Aris-Brosou S (2005) Determinants of adaptive evolution at the molecular level: the extended complexity hypothesis. Mol Biol Evol 22(2):200–209. https://doi.org/10.1093/molbev/msi006
Ballouz S, Francis AR, Lan R, Tanaka MM (2010) Conditions for the evolution of gene clusters in bacterial genomes. PLoS Comput Biol 6(2):e1000672. https://doi.org/10.1371/journal.pcbi.1000672
Borenstein E, Shlomi T, Ruppin E, Sharan R (2007) Gene loss rate: a probabilistic measure for the conservation of eukaryotic genes. Nucleic Acids Res 35(1):e7. https://doi.org/10.1093/nar/gkl792
Bottery MJ, Wood AJ, Brockhurst MA (2017) Adaptive modulation of antibiotic resistance through intragenomic coevolution. Nat Ecol Evol 1(9):1364–1369. https://doi.org/10.1038/s41559-017-0242-3
Brochier C, Philippe H, Moreira D (2000) The evolutionary history of ribosomal protein RpS14: horizontal gene transfer at the heart of the ribosome. Trends Genet 16(12):529–533. https://doi.org/10.1016/S0168-9525(00)02142-9
Brunet TDP, Doolittle WF (2018) The generality of constructive neutral evolution. Biol Philos 33(1):2. https://doi.org/10.1007/s10539-018-9614-6
Carlson MRJ, Zhang B, Fang Z, Mischel PS, Horvath S, Nelson SF (2006) Gene connectivity, function, and sequence conservation: predictions from modular yeast co-expression networks. BMC Genom 7(1):40. https://doi.org/10.1186/1471-2164-7-40
Chamosa LS, Álvarez VE, Nardelli M, Quiroga MP, Cassini MH, Centrón D (2017) Lateral antimicrobial resistance genetic transfer is active in the open environment. Sci Rep 7(1):513. https://doi.org/10.1038/s41598-017-00600-2
Charlesbois RL, Doolittle WF (2004) Computing prokaryotic gene ubiquity: rescuing the core from extinction. Genome Res 14(12):2469–2477. https://doi.org/10.1101/gr.3024704
Cohen O, Gophna U, Pupko T (2011) The complexity hypothesis revisited: connectivity rather than function constitutes a barrier to horizontal gene transfer. Mol Biol Evol 28(4):1481–1489. https://doi.org/10.1093/molbev/msq333
Cohen O, Gophna U, Pupko T (2013) The complexity hypothesis and other connectivity barriers to lateral gene transfer. In: Gophna U (ed) Lateral gene transfer in evolution. Springer, New York, pp 137–145
Coleman W (1964) Georges Cuvier, zoologist: a study in the history of evolutionary theory. Harvard University Press, Cambridge
Condit R (1990) The evolution of transposable elements: conditions for establishment in bacterial populations. Evol 44(2):347–359. https://doi.org/10.1111/j.1558-5646.1990.tb05204.x
Condit R, Stewart FM, Levin BR (1988) The population biology of bacterial transposons: a priori conditions for maintenance as parasitic DNA. Am Nat 132(1):129–147. https://doi.org/10.1086/284841
Cuvier G (1831) The animal kingdom arranged in conformity with its organization, 2nd edn, M’Murtrie H (trans). G & C & H Carvill, New York
Daubin V, Ochman H (2004) Bacterial genomes as new gene homes: the genealogy of ORFans in E. coli. Genome Res 14(6):1036–1042. https://doi.org/10.1101/gr.2231904
Davids W, Zhang Z (2008) The impact of horizontal gene transfer in shaping operons and protein interaction networks—direct evidence of preferential attachment. BMC Evol Biol 8(1):23. https://doi.org/10.1186/1471-2148-8-23
Doolittle WF (2010) The attempt on the life of the tree of life: science, philosophy and politics. Biol Philos 25(4):455–473. https://doi.org/10.1007/s10539-010-9210-x
Doolittle WF, Brown JR (1994) Tempo, mode, the progenote, and the universal root. P Natl A Sci USA 91(15):6721–6728. https://doi.org/10.1073/pnas.91.15.6721
Dutta C, Archana Pan (2002) Horizontal gene transfer and bacterial diversity. J Biosci 27(1):27–33. https://doi.org/10.1007/BF02703681
Francino MP (2012) The ecology of bacterial genes and the survival of the new. Int J Evol Biol 2012:394026. https://doi.org/10.1155/2012/394026
Franklin-Hall LR (2010) Trashing life’s tree. Biol Philos 25(4):689–709. https://doi.org/10.1007/s10539-010-9219-1
Fraser HB, Hirsh AE, Steinmetz LM, Scharfe C, Feldman MW (2002) Evolutionary rate in the protein interaction network. Science 296(5568):750–752. https://doi.org/10.1126/science.1068696
Frigaard N-U, Martinez A, Mincer TJ, DeLong EF (2006) Proteorhodopsin lateral gene transfer between marine planktonic bacteria and archaea. Nature 439(7078):847–850. https://doi.org/10.1038/nature04435
Giovannoni SJ, Bibbs L, Cho J-C, Stapels MD, Desiderio R, Vergin KL, Rappé MS et al (2005) Proteorhodopsin in the ubiquitous marine bacterium SAR11. Nature 438(7064):82–85. https://doi.org/10.1038/nature04032
Gophna U, Ofran Y (2011) Lateral acquisition of genes is affected by the friendliness of their products. P Natl A Sci USA 108(1):343–348. https://doi.org/10.1073/pnas.1009775108
Gumpert H, Kubicek-Sutherland JZ, Porse A, Karami N, Munck C, Linkevicius M, Adlerberth I, Wold AE, Andersson DI, Sommer MOA (2017) Transfer and persistence of a multi-drug resistance plasmid in situ of the infant gut microbiota in the absence of antibiotic treatment. Front Microbiol 8:1852. https://doi.org/10.3389/fmicb.2017.01852
Hao W, Golding GB (2006) The fate of laterally transferred genes: life in the fast lane to adaptation or death. Genome Res 16(5):636–643. https://doi.org/10.1101/gr.4746406
Itoh T, Takemoto K, Mori H, Gojobori T (1999) Evolutionary instability of operon structures disclosed by sequence comparisons of complete microbial genomes. Mol Biol Evol 16(3):332–346. https://doi.org/10.1093/oxfordjournals.molbev.a026114
Jain R, Rivera MC, Lake JA (1999) Horizontal gene transfer among genomes: the complexity hypothesis. P Natl A Sci USA 96(7):3801–3806. https://doi.org/10.1073/pnas.96.7.3801
Jain R, Rivera MC, Moore JE, Lake JA (2002) Horizontal gene transfer in microbial genome evolution. Theor Popul Biol 61(4):489–495. https://doi.org/10.1006/tpbi.2002.1596
Jordan IK, Wolf YI, Koonin EV (2003) No simple dependence between protein evolution rate and the number of protein-protein interactions: only the most prolific interactors tend to evolve slowly. BMC Evol Biol 3(1):1. https://doi.org/10.1186/1471-2148-3-1
Kacar B, Garmendia E, Tuncbag N, Andersson DI, Hughes D (2017) Functional constraints on replacing an essential gene with its ancient and modern homologs. MBio 8(4):e01276-17. https://doi.org/10.1128/mBio.01276-17
Lawrence JG (1999) Selfish operons: the evolutionary impact of gene clustering in prokaryotes and eukaryotes. Curr Opin Genet Dev 9(6):642–648. https://doi.org/10.1016/S0959-437X(99)00025-8
Lawrence JG, Roth JR (1996) Selfish operons: horizontal transfer may drive the evolution of gene clusters. Genetics 143(4):1843–1860
Lercher MJ, Pál C (2008) Integration of horizontally transferred genes into regulatory interaction networks takes many million years. Mol Biol Evol 25(3):559–567. https://doi.org/10.1093/molbev/msm283
Lewontin RC (1970) The units of selection. Ann Rev Ecol Syst 1(1):1–18. https://doi.org/10.1146/annurev.es.01.110170.000245
Loftie-Eaton W, Bashford K, Quinn H, Dong K, Millstein J, Hunter S, Thomason MK, Merrikh H, Ponciano JM, Top EM (2017) Compensatory mutations improve general permissiveness to antibiotic resistance plasmids. Nat Ecol Evol 1(9):1354–1363. https://doi.org/10.1038/s41559-017-0243-2
Majewski J, Cohan FM (1998) The effect of mismatch repair and heteroduplex formation on sexual isolation in Bacillus. Genetics 148:13–18
Majewski J, Zawadzki P, Pickerill P, Cohan FM, Dowson CG (2000) Barriers to genetic exchange between bacterial species: Streptococcus pneumoniae transofmration. J Bacteriol 182(4):1016–1023. https://doi.org/10.1128/JB.182.4.1016-1023.2000
Makino T, Gojobori T (2007) Evolution of protein-protein interaction network. In: Volff J-N (ed) Gene and protein evolution. Karger, Basil, pp 13–29. https://doi.org/10.1159/000107601
Mira A, Ochman H, Moran NA (2001) Deletional bias and the evolution of bacterial genomes. Trends Genet 17(10):589–596. https://doi.org/10.1016/S0168-9525(01)02447-7
Morris JJ, Lenski RE, Zinser ER (2012) The black queen hypothesis: evolution of dependencies through adaptive gene loss. MBio 3(2):e00036-12. https://doi.org/10.1128/mBio.00036-12
Mulkidjanian AY, Koonin EV, Makarova KS, Mekhedov SL, Sorokin A, Wolf YI, Dufresne A et al (2006) The cyanobacterial genome core and the origin of photosynthesis. P Natl A Sci USA 103(35):13126–13131. https://doi.org/10.1073/pnas.0605709103
Nelson KE, Clayton RA, Gill SR, Gwinn ML, Dodson RJ, Haft DH, Hickey EK et al (1999) Evidence for lateral gene transfer between archaea and bacteria from genome sequence of Thermotoga maritima. Nature 399(6734):323–329. https://doi.org/10.1038/20601
Novick A (2019) Cuvierian functionalism. Phil Theor Pract Biol 11:20190821. https://doi.org/10.3998/ptpbio.16039257.0011.005
Omelchenko MV, Makarova KS, Wolf YI, Rogozin IB, Koonin EV (2003) Evolution of mosaic operons by horizontal gene transfer and gene displacement in situ. Genome Biol 4(9):R55. https://doi.org/10.1186/gb-2003-4-9-r55
Outram D (1986) Uncertain legislator: Georges Cuvier’s laws of nature in their intellectual context. J Hist Biol 19(3):323–368. https://doi.org/10.1007/BF00138285
Pál C, Hurst LD (2004) Evidence against the selfish operon theory. Trends Genet 20(6):232–234. https://doi.org/10.1016/j.tig.2004.04.001
Pál C, Papp B, Lercher MJ (2005) Adaptive evolution of bacterial metabolic networks by horizontal gene transfer. Nat Genet 37(12):1372–1375. https://doi.org/10.1038/ng1686
Paquola ACM, Asif H, Pereira CAB, Feltes BC, Bonatto D, Lima WC, Mench CFM (2018) Horizontal gene transfer building prokaryote genomes: genes related to exchange between cell and environment are frequently transferred. J Mol Evol 86(3):190–203. https://doi.org/10.1007/s00239-018-9836-x
Park C, Zhang J (2012) High expression hampers horizontal gene transfer. Genome Biol Evol 4(4):523–532. https://doi.org/10.1093/gbe/evs030
Peter IS, Davidson EH (2015) Genomic control process: development and evolution. Academic Press, San Diego
Price MN, Huang KH, Arkin AP, Alm EJ (2005) Operon formation is driven by co-regulation and not by horizontal gene transfer. Genome Res 15(6):809–819. https://doi.org/10.1101/gr.3368805
Rudwick MJS (1997) Georges Cuvier, fossil bones, and geological catastrophes. University of Chicago Press, Chicago
Russell ES (1982) Form and function: a contribution to the history of animal morphology. University of Chicago Press, Chicago
Sato M, Miyazaki K (2017) Phylogenetic network analysis revealed the occurrence of horizontal gene transfer of 16S rRNA in the genus Enterobacter. Front Microbiol 8:2225. https://doi.org/10.3389/fmicb.2017.02225
Schank JC, Wimsatt WC (1986) Generative entrenchment and evolution. PSA PSer 2:33–60. https://doi.org/10.1086/psaprocbienmeetp.1986.2.192789
Schwenk K, Wagner GP (2001) Function and the evolution of phenotypic stability: connecting pattern to process. Integr Comp Biol 41(3):552–563. https://doi.org/10.1093/icb/41.3.552
Sharma AK, Spudich JL, Doolittle WF (2006) Microbial rhodopsins: functional versatility and genetic mobility. Trends Microbiol 14(11):463–469. https://doi.org/10.1016/j.tim.2006.09.006
Sober E (1984) The nature of selection. University of Chicago Press, Chicago
Soucy SM, Huang J, Gogarten JP (2015) Horizontal gene transfer: building the web of life. Nat Rev Genet 16(8):472–482. https://doi.org/10.1038/nrg3962
Stoltzfus A (1999) On the possibility of constructive neutral evolution. J Mol Evol 49(2):169–181. https://doi.org/10.1007/PL00006540
Stoltzfus A (2012) Constructive neutral evolution: exploring evolutionary theory’s curious disconnect. Biol Direct 7(1):35. https://doi.org/10.1186/1745-6150-7-35
Swithers KS, Soucy SM, Gogarten JP (2012) The role of reticulate evolution in creating innovation and complexity. Int J Evol Biol 2012:418964. https://doi.org/10.1155/2012/418964
Tian R-M, Cai L, Zhang W-P, Cao H-L, Qian P-Y (2015) Rare events of intragenus and intraspecies horizontal transfer of the 16S rRNA gene. Genome Biol Evol 7(8):2310–2320. https://doi.org/10.1093/gbe/evv143
Tsukuda M, Kitahara K, Miyazaki K (2017) Comparative RNA function analysis reveals high functional similarity between distantly related bacterial 16S rRNAs. Sci Rep 7(1):1–8. https://doi.org/10.1038/s41598-017-10214-3
Van Valen L (1971) Group selection and the evolution of dispersal. Evol 25(4):591–598. https://doi.org/10.1111/j.1558-5646.1971.tb01919.x
Vulic M, Dionisio F, Taddei F, Radman M (1997) Molecular keys to speciation: DNA polymorphism and the control of genetic exchange in Enterobacteria. P Natl A Sci USA 94(18):9763–9767. https://doi.org/10.1073/pnas.94.18.9763
Wagner GP, Schwenk K (2000) Evolutionarily stable configurations: functional integration and the evolution of phenotypic stability. In: Hecht MK, Macintyre RJ, Clegg MT (eds) Evolutionary biology. Springer, Boston, pp 155–217. https://doi.org/10.1007/978-1-4615-4185-1_4
Watanabe T (1963) Infective heredity of multiple drug resistance in bacteria. Bacteriol Rev 27(1):87–115
Wellner A, Lurie MN, Gophna U (2007) Complexity, connectivity, and duplicability as barriers to lateral gene transfer. Genome Biol 8(8):R156. https://doi.org/10.1186/gb-2007-8-8-r156
Wideman JG, Novick A, Muñoz-Gómez SA, Doolittle WF (2019) Neutral evolution of cellular phenotypes. Curr Opin Genet Dev 59:87–94. https://doi.org/10.1016/j.gde.2019.09.004
Wimsatt WC (1986) Developmental constraints, generative entrenchment, and the innate-acquired distinction. In: Bechtel W (ed) Integrating scientific disciplines. Martinus Nijhoff Publishers, Dordrect, pp 185–208
Wimsatt WC (2013a) Evolution and the stability of functional architectures. In: Huneman P (ed) Functions: selection and mechanisms. Springer, Dordrecht, pp 19–41. https://doi.org/10.1007/978-94-007-5304-4_2
Wimsatt WC (2013b) The role of generative entrenchment and robustness in the evolution of complexity. In: Lineweaver CH (ed) Complexity and the arrow of time. Cambridge University Press, Cambridge, pp 308–331. https://doi.org/10.1017/CBO9781139225700.017
Wimsatt WC (2013c) Entrenchment and scaffolding: an architecture for a theory of cultural change. In Caporael LR, Griesemer JR, Wimsatt WC (eds). The MIT Press, Cambridge, MA, pp 77-105
Wimsatt WC (2015) Entrenchment as a theoretical tool in evolutionary developmental biology. In: Love AC (ed) Conceptual change in biology: scientific and philosophical perspectives on evolution and development. Springer, Dordrecht, pp 365–402. https://doi.org/10.1007/978-94-017-9412-1_17
Woese CR, Gibson J, Fox GE (1980) Do genealogical patterns in purple photosynthetic bacteria reflect interspecific gene transfer? Nature 283(5743):212–214. https://doi.org/10.1038/283212a0
Wright GD (2010) Antibiotic resistance in the environment: a link to the clinic? Curr Opin Microbiol 13(5):589–594. https://doi.org/10.1016/j.mib.2010.08.005
Wu Z-W, Wang Q-M, Liu X-Z, Bai F-Y (2016) Intragenomic polymorphism and intergenomic recombination in the ribosomal RNA genes of strains belonging to a yeast species Pichia membranifaciens. Mycol 7(3):102–111. https://doi.org/10.1080/21501203.2016.1204369
Acknowledgments
The authors would like to thank Bill Wimsatt, Joe Bielawski, Fabien Denis-Cayer, Maureen O’Malley, and two anonymous referees for Biology and Philosophy for comments on the manuscript, as well as Jeremy Wideman and Chris Jones for helpful discussion. This work was supported by the Natural Sciences and Engineering Research Council of Canada, Grant Number GLDSU/447989.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Novick, A., Doolittle, W.F. Horizontal persistence and the complexity hypothesis. Biol Philos 35, 2 (2020). https://doi.org/10.1007/s10539-019-9727-6
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10539-019-9727-6