Joan Roughgarden

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Joan Roughgarden
Born (1946-03-13) 13 March 1946 (age 77)
Paterson, New Jersey, U.S.
Alma mater University of Rochester
Known forCritiques of sexual selection, theory of social selection
Scientific career
Fields Ecology and evolutionary biology
Institutions University of Massachusetts Boston
Stanford University
Hawaiʻi Institute of Marine Biology
Thesis Implications of density dependent natural selection  (1971)

Joan Roughgarden (born 13 March 1946) is an American ecologist and evolutionary biologist. She has engaged in theory and observation of coevolution and competition in Anolis lizards of the Caribbean, and recruitment limitation in the rocky intertidal zones of California and Oregon. She has more recently become known for her rejection of sexual selection, her theistic evolutionism, and her work on holobiont evolution.

Contents

Personal life and education

Roughgarden was born in Paterson, New Jersey, United States. She received a Bachelor of Science in biology (with Distinction and Phi Beta Kappa) and a Bachelor of Arts in Philosophy with highest honors from University of Rochester in 1968 and later a Ph.D. in biology from Harvard University in 1971. In 1998, Roughgarden came out as transgender and changed her name to Joan, making a coming out post on her website on her 52nd birthday. [1]

Career

Roughgarden worked as an instructor and Assistant Professor of Biology at the University of Massachusetts Boston from 1970 to 1972. In 1972 she joined the faculty of the Department of Biology at Stanford University. After becoming full professor she retired in 2011, and became Emeritus Professor. She founded and directed the Earth Systems Program at Stanford and has received awards for service to undergraduate education. In 2012 she moved to Hawaii, where she became an adjunct professor at the Hawaiʻi Institute of Marine Biology. In her academic career, Roughgarden advised 20 Ph.D. students and 15 postdoctoral fellows. [2]

Roughgarden has authored books and over 180 scientific articles. In addition to a textbook on ecological and evolutionary theory in 1979, Roughgarden has carried out ecological field studies with Caribbean lizards and with barnacles and their larvae along the California coast. In 2015, she wrote the fiction novel Ram-2050, a science-fiction retelling of the Ramayana.

Research

Caribbean Anoles & Interspecific Competition

Roughgarden's early work in the 1970s and 80s helped to develop the Anolis lizards of the Caribbean as an important model system for evolution and ecology. For example, she used two-species enclosure experiments on two Caribbean islands to demonstrate increasing strength of interspecific competition as resource partitioning decreases: [3] a central tenet for competition theory. The Anolis system thus provided an early example of an eco-evolutionary feedback, [4] and with further development by Jonathan Losos and others, has become an important example of adaptive radiation.

Barnacles & Recruitment Limitation

After setting up a lab at the Hopkins Marine Station, Roughgarden sought to extend her approach of combining theoretical with field research by studying intertidal acorn barnacles ( Balanus and Chthamalus spp). Earlier work by Joseph Connell, Bob Paine and others had suggested that the characteristic zonation of rocky intertidal communities was predominantly structured by predation, [5] (for example by Pisaster seastars) and by competition, [6] [7] wherein dominant Balanus species displaced Chthamalus species to the high intertidal zones. Together with her student, Steve Gaines, Roughgarden showed that these interspecific interactions were most important in intertidal localities and communities with a high density of barnacles, such as those Connell and others had studied in Scotland. [6] [8] At Hopkins in Central California, however, barnacle density was lower, and the amount of free space was best explained by periodic pulses of larval recruitment. [8]  With her student Sean Connolly, she then showed, through both empirical observation and modeling, that a latitudinal gradient in upwelling along the west coast of North America created very dense barnacle recruitment in the north (Oregon and Washington), where upwelling was weak, and very sparse barnacle recruitment in the south (California), where upwelling was strong. [9] This in turn explained why field studies in the north had found interspecific interactions to be important, while her own field studies in the south had found larval recruitment to be most important for structuring intertidal populations. [10] This deft synthesis helped to drive a paradigm shift in marine ecology which emphasized larval dispersal and recruitment dynamics over adult interactions and favored demographic models of populations open to larval recruits from distant localities, which dominated the field during the 1990s. [11]

Criticism of sexual selection

Around the time of her transition, Roughgarden began to shift her research focus to Darwin’s theory of sexual selection. In her 2004 book, Evolution’s Rainbow, [12] Roughgarden analyzes how biology can influence human sexuality and gender identity and explores the substantial diversity of mating systems and sexuality throughout the animal kingdom, with an eye toward understanding human sexual categories like gay, lesbian, and trans. In this book, and other articles around the same time, she offered criticism of sexual selection theory [13] [14] [15] by providing examples of species that depart from its predictions (such as homosexual behavior in bonobos, elephants and lizards) as well as highlighting contradictions between population genetic theory and sexual selection theory. She also provided the beginnings of an alternative theory to sexual selection called social selection, which she describes as being focused on natural selection based on differential offspring production, where sexual selection is focused on differential mating success.

A 2006 article in the journal Science with her student Erol Akçay, and Meeko Oishi, formally presented the theory of social selection in terms of game theory. [16] Beyond the Nash Competitive Equilibrium (NCE) imported to evolutionary biology by John Maynard Smith as the Evolutionary Stable Strategy, Roughgarden et al. discuss the Nash Bargaining Solution (NBS), which exists as an alternative to the NCE that is reached through negotiation. When playing in developmental time (as opposed to evolutionary time), a game player that stands to lose individual fitness at an NCE relative to its competitor may establish a threat point by promising to play a sub-optimal strategy. Through negotiation, for example via a side payment, the players can arrive at an NBS through playing mixed strategies across repeated games which thereby maximizes the fitness of the cooperative "team" (which consists of both players) rather than to any one player. Roughgarden et al. provide several examples of what such cooperative game play would look like in nature, and then define the evolutionary theory of social selection as one which considers such cooperative team games in the developmental tier as the primitive state, with sexual conflict as the derived state. They argue that social selection theory is mutually exclusive with the evolutionary theory of sexual selection, which treats sexual conflict as the primitive state and sexual cooperation as derived.

Following the Science paper, forty scientists produced ten critical letters [17] [18] stating that the article was misleading, that it contained misunderstandings and misrepresentations, that sexual selection accounted for all the data presented and subsumed Roughgarden's theoretical analysis, and that sexual selection explained data that her theory could not. [17] [18] Troy Day stated that "many people felt that this was completely shoddy science and poor scholarship, all motivated by a personal agenda". [17] Roughgarden stated she was "not altogether surprised" by the volume of dissent and that her theory was not an extension of sexual selection theory. [17] [18]

Tim Clutton-Brock of Oxford University wrote a more detailed rebuttal in Science in 2007, [19] in which he concedes the point that males can engage in sexual selection on females, even in species where the operational sex ratio is biased towards males, stating: "Consequently, satisfactory explanations of the evolution of sex differences requires an understanding of the operation of sexual selection in females as well as males". [19] Nevertheless, Clutton-Brock concludes that sexual selection is a robust theoretical framework, without ever addressing the theoretical distinction in the polarity of intersexual cooperation and conflict highlighted by Roughgarden et al. [16]

In her 2009 book The Genial Gene, [20] Roughgarden continues to build a case against sexual selection theory and to present social selection theory as an alternative. The book is titled as a response to the popular book, The Selfish Gene, by Richard Dawkins, [21] which expounds what Roughgarden describes a “neo-Spencerian” view of nature “red in tooth and claw” in which competition and conflict dominate. In The Genial Gene, after an initial section defining and attacking sexual selection, followed by a definition of social selection as one based on differences in offspring-production, rather than differences in mating success.

A second section is focused on the genetic basis of social selection. The first chapter addresses how sexual reproduction evolved in the first place, and makes the case for Roughgarden’s Portfolio hypothesis, which emphasizes that sexual reproduction creates genetic diversity through recombination, as opposed to the more commonly favored Muller’s Ratchet, which emphasizes that sex removes deleterious mutations through recombination. The second chapter explains the binary distribution of gamete types (sperm vs. egg) as a strategy to maximize gametic contact, rather than as a result of conflicting gametic strategies. A final chapter argues that hermaphroditism, rather than gonochorism, is the primitive state of sexuality.

The third section takes a two-tier approach to developing social selection theory. A behavioral tier focuses on game theory and Nash Bargaining Solutions as outlined in her 2006 paper. [16] A second population genetic tier is then described that operates as a result of many replays of the behavioral tier.  The book concludes by listing 26 phenomena that, according to Roughgarden, are explained differently by sexual selection theory and are better explained by social selection theory. She says that sexual selection theory derives from a view of natural behavior predicated on the selfish-gene concept, competition and deception, whereas the social-selection theory derives from teamwork, honesty, and genetic equality. As of 2012 she has continued to study if social selection as opposed to sexual selection is a more important driver of evolution for colonial species such as corals or perhaps humans. [22] [23]

Roughgarden's criticism of sexual selection has been rejected by the scientific community, and her papers on it have received few citations in scientific literature. [24] In a 2019 interview, she stated that "Most biologists remain defensive of sexual selection theory”. [15]

In 2013, Roughgarden funded a Catalysis meeting at the National Evolutionary Synthesis Center with the goal of debating and reviewing "the status of sexual selection studies and to indicate challenges and future directions". [25] The group struggled to come to a consensus definition of sexual selection, but a subgroup offered a definition that for the first time explicitly differentiated fecundity selection for sexual selection sensu stricto. [25]

Theistic evolution

Roughgarden has written on the relationship between Christianity and science. [26] Her book Evolution and Christian Faith: Reflections of an Evolutionary Biologist presents scripture passages that emphasize her belief that the Bible does not conflict with evolutionary biology and relates Christianity and evolution by asserting that all life is interconnected, as members of a faith community are connected. Roughgarden opposes creationism and intelligent design, but asserts her belief in God's involvement in evolution. [27] She was a speaker at the Beyond Belief symposium in 2006. [28]

Holobiont Evolution

As professor emerita, Dr. Roughgarden turned her attention to the emerging concept of the holobiont, which she defined as “an animal or plant host together with all the microbes living on or in it, exosymbionts and endosymbionts, respectively. [29] ” The concept, which originated in 1943, has had increasing recognition with the rise of second and third-generation DNA sequencing methods that allow the microbial communities (i.e. the microbiome) of a host to be examined. The close association between the microbiome and its host has led many [30] [31] [32]  to suggest that the holobiont may be an evolutionary unit of selection, in which the combination of the host’s genes with those of its microbiome produce an extended genome, or hologenome. However, the hologenome concept has been criticized on the grounds that microbiomes are usually not vertically transmitted from parent to child, [33] thereby violating what is commonly thought to be one of the key principles of natural selection: variation inherited in a Mendelian fashion.

Together with other proponents of the holobiont concept, Roughgarden wrote a 2018 review of the topic [29] in which they examined the evidence for the holobiont as a biological entity. They considered the tight integration of physiological, developmental, reproductive and even immunological components between host and microbial symbionts to provide a foundation for this concept. For example mammalian mothers’ milk contains sugars that appear to be for the benefit of the microbial symbionts, because they cannot be metabolized by the newborn. [34]  They also cite the horizontal acquisition of DNA coding for syncytin, [35] a protein that allows formation of the placenta, as a key step in the evolution of placental mammals, which also demonstrates adaptive evolution in the holobiont.

In this review, [29] Roughgarden begins to sketch a population genetic model of holobiont evolution, containing a host species, and a single microbial symbiont, and in which selection is based only on the number of copies of the symbiont genome acquired by the host. The model contains three sequential processes per generation: microbes can move between hosts, they can proliferate within hosts and holobionts can survive or perish dependent on the number of symbionts acquired. This model was enough to show that, with vertical transmission, a deleterious symbiont will reduce the number of holobionts (and symbionts), while a beneficial symbiont will tend to increase the sizes of both groups. However, horizontal transmission “binds the collection of microbiomes into a unified system, a meta-community, rather than a collection of independent communities”.

Roughgarden followed this review with two papers [36] [37] that further fleshed out her model of holobiont evolution. The first [36] showed that, when microbes colonize hosts following a Poisson distribution, horizontal transmission can still lead to holobiont evolution when beneficial symbionts increase the success of their hosts and thus flood the microbial source pool (the converse case with parasitic microbes also holds true). She calls this phenomenon “collective inheritance” as opposed to lineal Mendelian inheritance. The second paper [37] adds a second microbial species to the model, as well as a “colonization parameter” d, which partially determines the Poisson rate parameter. The d parameter approximates the density of the symbiont strain around the host, or the host’s selectivity for the symbiont species, depending on context. Because microbial colonization of the host follows a Poisson distribution, there is no Hardy-Weinberg analog, and directional selection tends to be more diffuse than expectated under vertical transmission. She then reasons from this two-microbe model that the host is likely to use antibodies and “probodies” to modulate d for each microbial species, in effect orchestrating things so that only microbes that provide some minimum amount of altruism toward their host are allowed to remain in symbiosis with the host. From the microbe’s standpoint, those species that provide the minimum amount of altruism to clear the host’s threshold will tend to outcompete those that provide more. This paper [37] carefully demonstrates that this host-orchestrated species selection process is conceptually distinct from co-evolution or multi-level selection and can predict and explain the tight integration of hosts and their microbial symbionts found throughout the eukaryotic tree of life.

Awards and honors

Roughgarden has served as associate editor of several academic journals, including Philosophy and Theory in Biology (since 2008), American Naturalist (1984–1989), Oecologia (1979–1982), and Theoretical Population Biology (1975–1986). She was the vice-chair and Chair of Theoretical Ecology Section of the Ecological Society of America during 2002–2003. She has served on the Nonprofit Organization Board for the Oceanic Society (San Francisco), the EPA Science Advisory Board Committee on Valuating the Protection of Ecological Systems and Services, and the science advisory boards of the Pacific Ocean Conservation Network (California), and the Channel Islands National Marine Sanctuary (Santa Barbara). [39]

Selected bibliography

Related Research Articles

<span class="mw-page-title-main">Symbiosis</span> Close, long-term biological interaction between distinct organisms (usually species)

Symbiosis is any type of a close and long-term biological interaction between two biological organisms of different species, termed symbionts, be it mutualistic, commensalistic, or parasitic. In 1879, Heinrich Anton de Bary defined it as "the living together of unlike organisms". The term is sometimes used in the more restricted sense of a mutually beneficial interaction in which both symbionts contribute to each other's support.

Horizontal transmission is the transmission of organisms between biotic and/or abiotic members of an ecosystem that are not in a parent-progeny relationship. This concept has been generalized to include transmissions of infectious agents, symbionts, and cultural traits between humans.

<span class="mw-page-title-main">Microbiota</span> Community of microorganisms

Microbiota are the range of microorganisms that may be commensal, mutualistic, or pathogenic found in and on all multicellular organisms, including plants. Microbiota include bacteria, archaea, protists, fungi, and viruses, and have been found to be crucial for immunologic, hormonal, and metabolic homeostasis of their host.

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The hologenome theory of evolution recasts the individual animal or plant as a community or a "holobiont" – the host plus all of its symbiotic microbes. Consequently, the collective genomes of the holobiont form a "hologenome". Holobionts and hologenomes are structural entities that replace misnomers in the context of host-microbiota symbioses such as superorganism, organ, and metagenome. Variation in the hologenome may encode phenotypic plasticity of the holobiont and can be subject to evolutionary changes caused by selection and drift, if portions of the hologenome are transmitted between generations with reasonable fidelity. One of the important outcomes of recasting the individual as a holobiont subject to evolutionary forces is that genetic variation in the hologenome can be brought about by changes in the host genome and also by changes in the microbiome, including new acquisitions of microbes, horizontal gene transfers, and changes in microbial abundance within hosts. Although there is a rich literature on binary host–microbe symbioses, the hologenome concept distinguishes itself by including the vast symbiotic complexity inherent in many multicellular hosts. For recent literature on holobionts and hologenomes published in an open access platform, see the following reference.

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<span class="mw-page-title-main">Phycosphere</span> Microscale mucus region that is rich in organic matter surrounding a phytoplankton cel

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<span class="mw-page-title-main">Microbiome</span> Microbial community assemblage and activity

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<span class="mw-page-title-main">Holobiont</span> Host and associated species living as a discrete ecological unit

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<span class="mw-page-title-main">Marine holobiont</span>

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References

  1. ↑ Yoon, Carol Kaesuk (October 17, 2000). "Scientist at Work: Joan Roughgarden; A Theorist With Personal Experience Of the Divide Between the Sexes". The New York Times. Retrieved March 7, 2014.
  2. ↑ "Curriculum Vitae: Joan Roughgarden". Stanford University. Retrieved March 7, 2014.
  3. ↑ Pacala, Stephen W.; Roughgarden, Jonathan (1985). "Population Experiments with the Anolis Lizards of St. Maarten and St. Eustatius". Ecology. 66 (1): 129–141. doi:10.2307/1941313. ISSN   1939-9170. JSTOR   1941313.
  4. ↑ Post, David M.; Palkovacs, Eric P. (June 12, 2009). "Eco-evolutionary feedbacks in community and ecosystem ecology: interactions between the ecological theatre and the evolutionary play". Philosophical Transactions of the Royal Society B: Biological Sciences. 364 (1523): 1629–1640. doi:10.1098/rstb.2009.0012. ISSN   0962-8436. PMC   2690506 . PMID   19414476.
  5. ↑ Paine, Robert T.; Vadas, Robert L. (1969). "The Effects of Grazing by Sea Urchins, Strongylocentrotus spp., on Benthic Algal Populations". Limnology and Oceanography. 14 (5): 710–719. Bibcode:1969LimOc..14..710P. doi: 10.4319/lo.1969.14.5.0710 .
  6. 1 2 Connell, Joseph H. (1961). "The Influence of Interspecific Competition and Other Factors on the Distribution of the Barnacle Chthamalus Stellatus". Ecology. 42 (4): 710–723. doi:10.2307/1933500. ISSN   0012-9658. JSTOR   1933500.
  7. ↑ Connell, Joseph H. (1961). "Effects of Competition, Predation by Thais lapillus, and Other Factors on Natural Populations of the Barnacle Balanus balanoides" . Ecological Monographs. 31 (1): 61–104. doi:10.2307/1950746. ISSN   0012-9615. JSTOR   1950746.
  8. 1 2 Gaines, S.; Roughgarden, J. (June 1, 1985). "Larval settlement rate: A leading determinant of structure in an ecological community of the marine intertidal zone". Proceedings of the National Academy of Sciences. 82 (11): 3707–3711. Bibcode:1985PNAS...82.3707G. doi: 10.1073/pnas.82.11.3707 . ISSN   0027-8424. PMC   397856 . PMID   16593571.
  9. ↑ Connolly, Sean R.; Roughgarden, Jonathan (April 1, 1998). "A Latitudinal Gradient in Northeast Pacific Intertidal Community Structure: Evidence for an Oceanographically Based Synthesis of Marine Community Theory". The American Naturalist. 151 (4): 311–326. doi:10.1086/286121. ISSN   0003-0147. PMID   18811323. S2CID   23831003.
  10. ↑ Connolly, Sean R.; Roughgarden, Joan (1999). "Theory of Marine Communities: Competition, Predation, and Recruitment-Dependent Interaction Strength". Ecological Monographs. 69 (3): 277–296. doi:10.1890/0012-9615(1999)069[0277:tomccp]2.0.co;2. ISSN   0012-9615.
  11. ↑ Caley, M. J.; Carr, M. H.; Hixon, M. A.; Hughes, T. P.; Jones, G. P.; Menge, B. A. (1996). "Recruitment and the Local Dynamics of Open Marine Populations". Annual Review of Ecology and Systematics. 27 (1): 477–500. doi:10.1146/annurev.ecolsys.27.1.477. ISSN   0066-4162. Archived from the original on January 31, 2022. Retrieved January 31, 2022.
  12. ↑ Roughgarden, Joan (2013). Evolution's rainbow : diversity, gender, and sexuality in nature and people (Tenth anniversary ed.). Berkeley. ISBN   978-0-520-95797-8. OCLC   861528157.{{cite book}}: CS1 maint: location missing publisher (link)
  13. ↑ Moser, Bob. "On the Originality of Species". Stanford Magazine. No. May/June 2004. Stanford University . Retrieved June 13, 2021.
  14. ↑ Jonah Lehrer. "The Effeminate Sheep". Seed (June/July 2006). Reprinted in Richard Preston, ed. (2007). The Best American Science and Nature Writing. New York: Houghton Mifflin. ISBN   978-0-618-72231-0.
  15. 1 2 "Q&A with Joan Roughgarden on the Problems with the Theory of Sexual Selection". MIT Press . February 11, 2019. Archived from the original on June 13, 2021. Retrieved June 13, 2021.
  16. 1 2 3 Roughgarden, Joan; Oishi, Meeko; Akçay, Erol (February 17, 2006). "Reproductive Social Behavior: Cooperative Games to Replace Sexual Selection". Science. 311 (5763): 965–969. Bibcode:2006Sci...311..965R. doi:10.1126/science.1110105. ISSN   0036-8075. PMID   16484485. S2CID   32364112.
  17. 1 2 3 4 Atkinson, Nick (May 5, 2006). "Sexual selection alternative slammed". The Scientist . Archived from the original on September 29, 2007. Retrieved May 15, 2007.
  18. 1 2 3 Dall, S. R. X.; McNamara, J. M.; Wedell, N.; Hosken, D. J. (May 5, 2006). "Debating Sexual Selection and Mating Strategies" (PDF). Science. 312 (5774): 689b–697b. doi:10.1126/science.312.5774.689b. PMID   16675684. S2CID   10887773 . Retrieved June 14, 2021.
  19. 1 2 Clutton-Brock, Tim (December 21, 2007). "Sexual Selection in Males and Females". Science. 318 (5858): 1882–1885. Bibcode:2007Sci...318.1882C. doi:10.1126/science.1133311. ISSN   0036-8075. PMID   18096798. S2CID   6883765.
  20. ↑ Roughgarden, Joan (2009). The genial gene : deconstructing Darwinian selfishness. Berkeley: University of California Press. ISBN   978-0-520-25826-6. OCLC   264039560.
  21. ↑ Dawkins, Richard. The selfish gene. OCLC   1238007082.
  22. ↑ Folse HJ, 3rd; Roughgarden, J (2010). "What is an individual organism? A multilevel selection perspective". The Quarterly Review of Biology. 85 (4): 447–72. doi:10.1086/656905. PMID   21243964. S2CID   19816447.{{cite journal}}: CS1 maint: numeric names: authors list (link)
  23. ↑ Roughgarden, J. (2012). "The social selection alternative to sexual selection". Philosophical Transactions of the Royal Society B: Biological Sciences. 367 (1600): 2294–2303. doi:10.1098/rstb.2011.0282. PMC   3391423 . PMID   22777017.
  24. ↑ Allen, Arthur (May 1, 2014). "Sexual Selection's Mystique Lingers". BioScience. 64 (5): 375–380. doi: 10.1093/biosci/biu047 . ISSN   0006-3568.
  25. 1 2 Roughgarden, Joan; Adkins-Regan, Elizabeth; Akçay, Erol; Crawford, Jeremy Chase; Gadagkar, Raghavendra; Griffith, Simon C.; Hinde, Camilla A.; Hoquet, Thierry; O’Connor, Cailin; Prokop, Zofia M.; Prum, Richard O. (January 10, 2015), Sexual selection studies: a NESCent catalyst meeting, doi: 10.7287/peerj.preprints.680v3 , S2CID   14039177
  26. ↑ "First Congregational Church of Berkeley: Event Details". Archived from the original on October 8, 2007. Retrieved September 19, 2006.
  27. ↑ Roughgarden, Joan. Evolution and Christian Faith: Reflections of an Evolutionary Biologist. Washington D.C.: Island Press, 2006.
  28. ↑ "TSN: Beyond Belief: Science, Reason, Religion & Survival". thesciencenetwork.org. Retrieved September 27, 2016.
  29. 1 2 3 Roughgarden, Joan; Gilbert, Scott F.; Rosenberg, Eugene; Zilber-Rosenberg, Ilana; Lloyd, Elisabeth A. (2018). "Holobionts as Units of Selection and a Model of Their Population Dynamics and Evolution". Biological Theory. 13 (1): 44–65. doi: 10.1007/s13752-017-0287-1 . ISSN   1555-5542. S2CID   256282704.
  30. ↑ Bordenstein, Seth R.; Theis, Kevin R. (August 18, 2015). "Host Biology in Light of the Microbiome: Ten Principles of Holobionts and Hologenomes". PLOS Biology. 13 (8): e1002226. doi: 10.1371/journal.pbio.1002226 . ISSN   1545-7885. PMC   4540581 . PMID   26284777.
  31. ↑ Rosenberg, Eugene; Zilber-Rosenberg, Ilana (May 4, 2016). Collier, R. John (ed.). "Microbes Drive Evolution of Animals and Plants: the Hologenome Concept". mBio. 7 (2): e01395. doi:10.1128/mBio.01395-15. ISSN   2161-2129. PMC   4817260 . PMID   27034283.
  32. ↑ Gilbert, Scott F.; Sapp, Jan; Tauber, Alfred I. (2012). "A Symbiotic View of Life: We Have Never Been Individuals". The Quarterly Review of Biology. 87 (4): 325–341. doi:10.1086/668166. ISSN   0033-5770. PMID   23397797. S2CID   14279096.
  33. ↑ Moran, Nancy A.; Sloan, Daniel B. (December 4, 2015). "The Hologenome Concept: Helpful or Hollow?". PLOS Biology. 13 (12): e1002311. doi: 10.1371/journal.pbio.1002311 . ISSN   1545-7885. PMC   4670207 . PMID   26636661.
  34. ↑ Yoshida, Erina; Sakurama, Haruko; Kiyohara, Masashi; Nakajima, Masahiro; Kitaoka, Motomitsu; Ashida, Hisashi; Hirose, Junko; Katayama, Takane; Yamamoto, Kenji; Kumagai, Hidehiko (September 16, 2011). "Bifidobacterium longum subsp. infantis uses two different β-galactosidases for selectively degrading type-1 and type-2 human milk oligosaccharides". Glycobiology. 22 (3): 361–368. doi: 10.1093/glycob/cwr116 . ISSN   1460-2423. PMID   21926104.
  35. ↑ Dupressoir, A.; Lavialle, C.; Heidmann, T. (2012). "From ancestral infectious retroviruses to bona fide cellular genes: Role of the captured syncytins in placentation". Placenta. 33 (9): 663–671. doi:10.1016/j.placenta.2012.05.005. ISSN   0143-4004. PMID   22695103.
  36. 1 2 Roughgarden, Joan (March 2, 2020). "Holobiont Evolution: Mathematical Model with Vertical vs. Horizontal Microbiome Transmission". Philosophy, Theory, and Practice in Biology. 12 (20220112). doi: 10.3998/ptpbio.16039257.0012.002 . hdl:2027/spo.16039257.0012.002. ISSN   2475-3025. S2CID   216329421.
  37. 1 2 3 Roughgarden, Joan (June 1, 2023). "Holobiont Evolution: Population Theory for the Hologenome". The American Naturalist. 201 (6): 763–778. doi: 10.1086/723782 . ISSN   0003-0147. PMID   37229712. S2CID   220253227.
  38. ↑ "Lloyd W. Dinkelspiel Awards | Registrar's Office". registrar.stanford.edu. Retrieved April 4, 2019.
  39. ↑ "Science Matters". California Science Center. Archived from the original on July 13, 2010.
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