Migration, admixture, and human populations

Mark L. Golitko


Please note: this commentary, recovered on 8-Jan-2017, was originally published by Mark L. Golitko on Science Dialogues on 30-Jun-2015.


Cellarius_ptolemaic_system
The Ptolemaic universe as depicted by Johannes van Loon, ca. 1611–1686.

TWO NEW STUDIES IN EUROPEAN PREHISTORY have recently made headlines. The first (Haak et al. 2015) purports to show, using genetic data from ancient skeletons, that massive migration from the Central Asian Steppes into Europe during the Bronze Age likely introduced Indo-European languages, thus supporting the venerable “Kurgan” hypothesis championed by Marija Gimbutas decades ago. The second study (Smith et al. 2015) identified DNA from domesticated wheat (triticum) in submarine peat deposits off the southern coast of England dating to 8000 years ago, two millennia before such plants formed an identifiable component of crop assemblages in known terrestrial sites in England, and thus well ahead of the Neolithic agricultural “front.”

The validity of the later results remains to be seen—the DNA in question was cored out of the ocean bottom, and while the published results appear robust, it is unlikely that these data will single-handedly overturn the long-standing archaeological narrative of the Neolithic. That study does however provide a convenient point of digression for reexamining the first study and other similar studies of ancient genetics. Archaeologists have typically used two kinds of models to explain the past—diffusionist models in which ideas, things, and practices move, and migrationist models in which ideas, things, and practices move because people move. The movement of domesticated plants and animals of Near Eastern origins into Europe—the so-called “Neolithic Revolution”—has been the bell-weather case for testing these two types of explanations in archaeology. In the last three decades or so, human genetics has entered the picture as a way of testing competing hypotheses, first using modern DNA samples from living people in Europe and the Near East, and increasingly in the last decade, using ancient DNA (aDNA) extracted from archaeological burials (Pinhasi et al. 2012).

European population genetics, modern and ancient

Early studies of modern biological patterning (initially using blood types and other proteins) suggested a broad SE-NW trend in frequencies (Ammermann and Cavalli-Sforza 1984), one that was later confirmed when DNA sequencing became possible. This pattern was immediately interpreted as the outcome of a Neolithic period migration out of the Near East into Europe beginning after 8000 BC, swamping out “indigenous” European peoples (and their genes) that had been in place since at least the end of the last ice age (c. 12,000 years ago or longer). Vigorous debate ensued as some researchers argued that this trend could have resulted from a much earlier peopling of Europe by modern humans c. 45,000 years ago, or possibly during the reoccupation of Europe after the last glacial maximum (c. 22,000 years ago) by people who had occupied glacial refugia further south in Europe (see Pinhasi et al. 2012 and Deguilloux et al. 2012 for reviews of this work).

In 2005, the first study of DNA from actual early Neolithic skeletons was published (Haak et al. 2005), and the results were quite different from what most researchers had expected. As it turns out, early Neolithic skeletons, at least in central Europe (associated with an archaeological culture called the Linienbandkeramik or LBK) contain gene frequencies that are quite unlike those found in modern European populations. Specifically, mitochondrial DNA (mtDNA) haplogroups (sets of genomes related by shared mutations at particular locations on the genome suggesting common origins) thought to be clear markers of Neolithic population growth and movement were only present at relatively low frequencies, while one particular haplogroup—N1a—present at extremely low frequencies anywhere in modern day Eurasia and Africa, was quite common in the early Neolithic genepool. In the ensuing ten years, there has been a rapidly growing set of aDNA analyses performed in Europe, both on mtDNA (tracing descent through females) and Y-chromosome aDNA (tracing descent through males). As with modern DNA, measuring descent through males and females provides somewhat different answers, and suggests that on a whole, women have been more mobile than men in Europe (likely indicating a very old predominant pattern of patrilocality, e.g., Seielstad et al. 1998). In some places (parts of Northern Spain, for instance—see Sampietro et al. 2007), early Neolithic gene frequencies are not that different from earlier ones or modern ones, while in central Europe at least, the early Neolithic did witness a massive reshaping of the genetic landscape from a relatively genetically homogenous late-Paleolithic and Mesolithic background to a much more diverse Neolithic one, and little similarity is evident between the Neolithic and the present day (see Pinhasi et al. 2012 and Deguilloux et al. 2012 for reviews of this work).

The Haak et al. study (published earlier this month) identifies gene flow between central Asia and Europe in the Bronze Age, and a series of other recent studies also clearly demonstrate that the Neolithic is not the end of the story either. The researchers postulate a massive migration of Steppe populations into Europe associated with the Yamnaya archaeological culture, one that has been previously hypothesized to have spread Indo-European languages both eastwards and westwards out of Central Asia. aDNA research is for the most part slowly hammering the nail in the coffin of diffusionist models for the spread of agriculture, and for many, is now offering strong support for the spread of languages through massive migratory events (including Renfrew’s [1988] hypothesized spread of Indo-European during the early Neolithic).

Human “populations”

Care needs to be taken in interpreting these results, however. Population geneticists model the human past as a series of admixture events between discrete populations (see Hellenthal et al. 2014 for a recent attempt to define how many such populations there are). These populations may be defined in a number of ways—by geography (typically by continent), by language, by self-defined or externally perceived ethnicity, and in the case of palaeogenetics, by archaeological culture. There is thus an “LBK” or a “PPNB” set of gene frequencies which can admix or not (see for instance Fernández et al. 2015). This is a convenient shorthand, because it allows a small number of analyses (aDNA studies have sampled at most a few hundred individuals to date, while even modern studies are based on only thousands of individuals) to be taken as representative of some larger analytically meaningful population.

By Mike88n (Mike88n) [GPL (http://www.gnu.org/licenses/gpl.html)], via Wikimedia Commons (originally from Novembre et al. 2008).
Modern genetic map of Europe. (By Mike88n (Mike88n) [GPL (http://www.gnu.org/licenses/gpl.html)], via Wikimedia Commons (originally from Novembre et al. 2008)).

But what is a human population? That we have many ways of categorizing each other is unquestioned—we divide people up by race, income, clothing style, dialect, neighborhood, country, and a thousand other ways. It is also not implausible to imagine that real geographical boundaries such as major mountain chains, oceans, deserts, and so forth, may produce long-term vicariant barriers inhibiting interaction (i.e., people having sex with one another). That this is so is clearly demonstrated by the fact that modern gene frequencies are strongly patterned by geography in Europe, so much so that a multi-dimensional scaling plot (a way of representing many axes of variability on a single two-dimensional plot) of gene frequencies virtually recreates the geographic shape of Europe (Novembre et al. 2008). It is also everyone’s experience that humans live in social groups that can feel very real and rigid, and thus it might seem clear that human populations can be defined. However, the issue in palaeogenetics is different, namely, whether people live in sexual groups impermeable and long-lasting enough to explain the long-term configuration and development of gene frequencies, as well as serving as the basic scaffolding for other forms of human identity including the transmission of learning through time (i.e., culture and languages, including Indo-European ones).

Analytical simplification and historical reality

If the goal is simply to abstractly model how genes may have moved across the landscape historically, then perhaps an analytical fiction of discrete human “populations” is adequate for the job, similar to the use of the “gene” as analytical shorthand for modeling the complex network of DNA-RNA-protein interactions that drive biological function (e.g., Dawkins 2009). In econometrics, Friedman (1970) argued that it didn’t matter whether models were based on plausible assumptions, as long as those theories generated testable predictions that matched observations and resulted in predictive power. However, while predictive power may result even from a model with unrealistic starting assumptions, if social scientists want to explain what actually happened, our starting assumptions do matter. Their plausibility must be evaluated by examining how consistent they are with our knowledge of the world, updated in light of new information—if those assumptions are subsequently found wanting, we must reject the basic plausibility of our models, even if they produce outcomes consistent with empirical data (Nooteboom 1986). This is simply another way of stating that the same outcome can often be generated by several different models, and we need to turn to other lines of information to choose between them. In a recent paper, Pickrell and Reich (2014) use simulation to demonstrate that a number of opposing population genetic models used to explain human genetic patterning can produce the exact same results when operating over long periods of time.

As more aDNA analyses are published, the number of population migrations required to explain observed palaeo- and modern-gene frequencies in Europe (and by implication elsewhere) appears to be steadily increasing, in some cases seemingly at a rate of one per study (e.g., Hervella et al. 2015). This situation reminds me somewhat of the addition of spheres to the Ptolemaic system of planetary motions. Eventually, the Ptolemaic system grew so ponderous that some doubted it merely on the principal of parsimony. It took a radical rethinking of planetary positioning to generate a far simpler explanation of planetary motion. In the case of palaeogenetics (and other explanations of the past), perhaps a similar shift in thinking is required, one that moves away from the monolithic “billiard-ball” model of cultures and populations to something more plausible.

The human network

What should be the unit of analysis in historical genetics (and historical explanation more generally), and how do we create models that are consistent with other observations about human social structure and sexual behavior? In other words, how do we distinguish between competing historical genetic models by evaluating the basic plausibility of those models? One promising avenue comes from the recent explosion of interest in network analysis, which provides a robust method and body of knowledge for describing human social structure and comparing it to genetic patterning (e.g., Terrell 2010), and which does not necessarily require that one define broader units of analysis in advance, such as archaeological cultures. The challenge is to combine our knowledge of network structure in the human population (small-worlds and the like) with our understanding of genetics to create more plausible models of the human past. How this is to be accomplished in a formal mathematical sense remains to be seen.

This is more than just an academic concern—the popular media picks up on these studies and reinforces the viewpoint that humans do in fact come in particular “types” that can be identified through the new science of genetics—for instance, a recent distillation of one such aDNA study in a major media outlet described the results as indicating that modern Europeans derive from “three tribes” of ancient people, one of whom may be previously “unknown” to science (Rincon 2014). Do we really need “pulse-stasis” models for human population structure in the past? How do we adequately account for the fact that archaeological evidence suggests expansive social networks wherever and whenever we look, and that modern political/continental boundaries and perceived historical and cultural areas are not adequate units of analysis for splitting populations then or now? What happens if we resample our data and begin arbitrarily drawing lines that don’t correspond to these perceived political, geographical, linguistic, or archaeological categories? Does the story stay the same? A social networks perspective on the past is one way to transcend these problematic but common-sense ideas of human population(s) structure. If wheat can move beyond “Neolithic” communities thousands of years earlier than previously supposed, what else was moving?

References

Dawkins, R. (2009) The Selfish Gene. Oxford, Oxford University Press.

Deguilloux, M.-F., R. Leahy, M.-H. Pemonge, and S. Rottier (2012) European Neolithization and Ancient DNA: An Assessment. Evolutionary Anthropology 21: 24-37.

Fernández, E., A. Pérez-Pérez, C. Gamba, E. Prats, P. Cuesta, J. Anfruns, M. Molist, E. Arroyo-Pardo, and D. Turbón (2014). Ancient DNA Analysis of 8000 B.C. Near Eastern Farmers Supports an Early Neolithic Pioneer Maritime Colonization of Mainland Europe through Cyprus and the Aegean Islands. PLoS Genetics 10(6): e1004401. doi:10.1371/journal.pgen.104401.

Friedman, M (1970) “The Methodology of Positive Economics.” In Essays on Positive Economics. Chicago: The University of Chicago Press, pp 1-43.

Haak, W., P. Forster, B. Bramanti, S. Matsumura, G. Brandt, M. Tänzer, R. Villems, C. Renfrew, D. Gronnborn, K. Werner Alt, and W. Burger. 2005. Ancient DNA from the First European Farmers in 7500-Year-Old Neolithic Sites. Science 310: 1016-1018.

Haak, W., I. Lazaridis, N. Patterson, N. Rohland, S. Mallick, B. Llamas, G. Brandt, S. Nordenfelt, E. Harney, K. Stewardson, Q. Fu, A. Mittnik, E. Bánffy, C. Economou, M. Francken, S. Friederich, R. Garrido Pena, F. Hallgren, V. Khartanovich, A. Khokholov, M. Kunst, P. Kuznetsov, H. Meller, O. Mochalov, V. Moiseyev, N. Nicklisch, S.L. Pichler, R. Risch, M.A. Rojo Guerra, C. Roth, A. Szécsényi-Nagy, J. Wahl, M. Meyer, J. Krause, D. Brown, D. Anthony, A. Cooper, K. Werner Alt, and D. Reich (2015) Massive migration from the steppe is a source for Indo-European languages in Europe. Nature522: 207-211.

Hellenthal, G., G.B.J. Busb, G. Band, J.F. Wilson, C. Capelli, D. Falush, and S. Myers (2014). A Genetic Atlas of Human Admixture History. Science 343: 747-751.

Hervella, M., M. Rotea, N. Izagirre, M. Constantinescu, S. Alonso, M. Ioana, C. Lazăr, F. Ridiche, A.D. Soficaru, M.G. Netea, and C. de-la-Rua (2015). Ancient DNA from South-East Europe Reveals Different Events during Early and Middle Neolithic Influencing the European Genetic Heritage. PLoS ONE 10(6):e0128810. Doi:10.1371/journal.pone.0128810.

Nooteboom, B (1986) Plausibility in Economics. Economics and Philosophy 2: 197-224.

Novembre, J., T. Johnson, K. Bryc, Z. Kutalik, A.R. Boyko, A. Auton, A. Indap, K.S. King, S. Bergmann, M.R. Nelson, M. Stephans, and C.D. Bustamante (2008) Genes mirror geography within Europe. Nature 456: 98-103.

Pinhasi, R., M.G. Thomas, M. Hofreiter, M. Currat, and J. Burger (2012) The genetic history of Europeans. Trends in Genetics 28(10): 496-505.

Renfrew, C. (1988) Archaeology & Language: the Puzzle of Indo-European Origins. Cambridge, Cambridge University Press.

Rincon, P. (2014) Europeans drawn from three ancient ‘tribes’ BBC News Science and Environment, 9/17/2014.

Sampietro, M.L., O. Lao, D. Caramelli, M. Lari, R. Pou, M. Martí, J. Bertranpetit, and C. Lalueza-Fox (2007) Palaeogenetic evidence supports a dual model of Neolithic spreading into Europe. Proceedings of the Royal Society B 274: 2161-2167.

Seielstad, M.T., E. Minch, and L.L. Cavalli-Sforza (1998) Genetic evidence for a higher female migration rate in humans. Nature Genetics 20: 278-280.

Smith, O., G. Momber, R. Bates, P. Garwood, S. Fitch, M. Pallen, V. Gaffney, and F.G. Allaby (2015) Sedimentary DNA from a submerged site reveals wheat in the British Isles 8000 years ago. Science 347: 998-1001.

Terrell, J.E. (2010) Social Network Analysis of the Genetic Structure of Pacific Islanders. Annals of Human Genetics 74: 211-232.

© Mark L. Golitko. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author(s) and source are credited. The statements and opinions expressed are those of the author(s) and do not constitute official statements or positions of the Editors and others associated with SCIENCE DIALOGUES.

 

Darwin’s use of “use” and “disuse” (Part 3)

Tom Clark


Please note: this commentary, recovered on 8-Jan-2017, was originally published by the author, Tom Clark, on Science Dialogues on 14-Mar-2015.


DARWIN IS CREDITED with dethroning humans from their special place between animals and angels. As Copernicus had done astronomically, so had Darwin biologically.

Feral_horses_-_Pryor_Mountain_Wild_Horse_Range_-_Montana
Pryor Mountain Wild Horse Range, Montana. http://www.blm.gov/pgdata/etc/medialib/blm/mt/blm_programs/whb.Par.0228.Image.198.149.1.gif

But Darwin achieved continuity of humans with animals as much by humanizing animals as shrinking humans. Resisting “the too-ready ascription of action to instinct” (Beer 2009: 242-255), Darwin imagined that horses “admired a wide prospect,” baboons had “capacious hearts,” earthworms made aesthetic choices, and snails showed “some degree of permanent attachment.” He did not imagine that biology could benefit, as physics had, by abandoning animism, animals being so . . . animistic.

It was the neo-Darwinian assumption that genes and environments were sufficient causes of animals’ behavior that turned natural selection from an animate doing into a physical happening. Attributing behavior to stable causes both inside (molecules) and outside (environment) turned animals into spectators, along for the ride. Their mental lives were made redundant in the British sense of unemployed. (Compare John and Gabriel Terrell’s thoughts about self-generated, stimulus-independent, internally directed thought in their March 3 post Thinking about Thinking 2. Through the Looking Glass.)

Misreading Darwin’s use of use and disuse as simply Lamarckian enabled the neo-Darwinian demotion of both humans and animals, as meaningful roles for ancestors and Gods were, like baby and bathwater, summarily thrown out.

The word purpose is singularly inapplicable to evolutionary change … If an organism is well adapted … this is not due to any purpose of its ancestors or of an outside agency, such as “Nature” or “God” … (Mayr 1961: 1504).

The purposeful activities of ancestors were not final or ultimate causes. They were some among many causes. Yet they were bundled with God’s finality and dismissed. In the last paragraph of Origin of Species (Darwin 1860: 490) between his “entangled bank” metaphor and the poetic “endless forms most beautiful,” Darwin summarized the key elements of his theory. Two have been pushed to the edges of mainstream evolutionary thought, the ultimate activities of “the Creator” and the contingent activities of ancestors—”use and disuse.”

In the margins of an article by Wallace, Darwin wrote “use of moral qualities” (Greene 1981: 102), telegraphing a view of our moral origins that insinuated these dignifying lines of descent:

  • Life is inherently autonomous.
  • Autonomy has evolved (Rosslenbroich 2014).
  • Nervous systems support flexible, adaptive responding.
  • Vertebrates specialized in intention, allowing metabolic support for increasingly larger brains (Wrangham 2009).
  • Birds and mammals made relationships vital heritable resources (Kemp 2006), expanding autonomy by cooperating in relationships of secure dependence and interdependence.
  • Humans extended these achievements with ethics (Boehm 2012) and friendship (Terrell 2015).

The twentieth century dethroning of humanity carried out in Darwin’s name clipped human dignity more than Darwin intended. The following affirmations return to the evolutionary image of ourselves buds of autonomy and responsibility that Darwin was careful to leave on our family tree.

affirmWhen we consider the evolutionary role of animal behavior—or as we also say, ancestors’ activities—scientific theory becomes human nature mythology, the telling of which must be recognized as a moral act (Bock 1994: 8). The moral significance of our origin story hits home with the realization that how we tell this story can leverage or constrain personal and collective action toward sustainability (Clark and Clark 2012), peace and justice (Chorover 1979; Oyama 2000; Novoa and Levine 2010).

The sense we make of ourselves and each other shapes who we become, including our capacities for learning, cooperation and self-regulation. “Knowing” that intelligence is fixed inhibits learning (Blackwell et al. 2007). “Knowing” that personality attributes are inherited impels hasty negative judgments of others, foreclosing opportunities for constructive encounter (Dweck 2000). “Knowing” that free will is illusory engenders cheating (Vohs and Schooler 2008) and aggression (Baumeister et al. 2009). “Knowing” that humans are selfish by nature favors policies that crowd out reciprocity and trust, inducing selfish behavior (Bowles 2008). And “knowing” that metabolism is natural while intention remains a supernatural specter (Mayr 1982) hedges responsibility for our extended metabolism—energy consumption—compromising our ability to regulate our own inventions.

Knowing there is a choice to make and it matters what we choose to do prepares us for wising up to shared responsibilities and cooperating in the good use of resources.

Biologists rightly argue that a clear understanding of our evolutionary past must inform our plans for a sustainable future (Vermeij 2010: 253). Explaining the evolution of sighted animals as a blind process blinkers our understanding of the past, so also our outlook. Envisioning and motivating sustainable living is better served by an origin story that includes the vision and intentions of ancestors.

Evolution is not only what happened to our ancestors while they were busy making other plans. Ancestors did not plan our evolution, but their plans, successful or not, with consequences intended or not, were part of the story.

In the way he used use and disuse, Darwin recognized our ancestors’ part in how we came to be and our part in resolving where we go from here. By affirming our autonomy and interdependence, Darwin’s origin story also demands of us continued use of our moral imaginations.

References

Baumeister, R. F., E. J. Masicampo, and C. N. DeWall (2009). Prosocial benefits of feeling free: disbelief in free will increases aggression and reduces helpfulness. Personality and Social Psychology Bulletin 35: 260–268.

Beer, G. (2009). Darwin’s Plots (3rd ed.). Cambridge: Cambridge University Press.

Blackwell, L. S., K. H. Trzesniewski, and C. S. Dweck (2007). Implicit theories of intelligence predict achievement across an adolescent transition: a longitudinal study and an intervention. Child Development 78: 246–263.

Bock, K. (1994). Human Nature Mythology. Urbana: University of Illinois Press.

Boehm, C. (2012). Moral Origins. New York: Basic Books.

Bowles, S. (2008). Policies designed for self-interested citizens may undermine ‘the moral sentiments’: evidence from economic experiments. Science 320: 94–112.

Chorover, S. L. (1979). From Genesis to Genocide. Cambridge: MIT Press.

Clark, T. and E. Clark (2012). Participation in evolution and sustainability. Transactions of the Institute of British Geographers 37: 563–577.

Darwin, C. R. (1860). On the Origin of Species (2d ed.). In J. van Wyhe, ed., 2002 The Complete Work of Charles Darwin Online(http://darwin-online.org.uk).

Dweck, C. S. (2000). Self Theories. Philadelphia: Psychology Press.

Greene, J. C. (1981). Science, Ideology, and World View. Berkeley: University of California Press.

Kemp, T. S. (2006). The origin of mammalian endothermy: A paradigm for the evolution of complex biological structure. Zoological Journal of the Linnean Society 147: 473–488.

Mayr E. (1961). Cause and effect in biology. Science 134, 3489: 1501–1506.

Mayr E. (1982). The Growth of Biological Thought. Cambridge: Harvard University Press.

Novoa, A. and A. Levine (2010). From Man to Ape. Chicago: University of Chicago Press.

Oyama, S. (2000). Evolution’s Eye. Durham: Duke University Press.

Rosslenbroich, B. (2014). On the Origin of Autonomy. Cham: Springer.

Terrell, J. E. (2015). A Talent for Friendship. Oxford: Oxford University Press.

Vermeij G. J. (2010). The Evolutionary World. New York: St. Martin’s Press.

Vohs, K. D. and J. W. Schooler (2008). The value of believing in free will: encouraging a belief in determinism increases cheating. Psychological Science 19: 49–54.

Wrangham, R. (2009). Catching Fire. New York: Basic Books.

Tom Clark

As a psychologist, I have been interested in the role of behavior in evolution since my graduate training at the University of South Florida.

 

 

© 2015, Thomas L. Clark. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author(s) and source are credited. The statements and opinions expressed in this article are those of the author(s) and do not constitute official statements or positions of the Editors and others associated with SCIENCE DIALOGUES.

 

 


Darwin’s use of “use” and “disuse” (Part 2)

Tom Clark


Please note: this commentary, recovered on 8-Jan-2017, was originally published by the author, Tom Clark, on Science Dialogues on 7-Mar-2015.


AT CHICAGO’S CENTENNIAL CELEBRATION of Origin of Species, Julian Huxley (1960: 14) attributed to Darwin this “Lamarckian error”:

… he did believe in the inheritance of certain “acquired characters”—the effects of the conditions of life and of use and disuse.

Though Darwin had been careful to use the terms use and disusedescriptively in Origin of Species, Huxley took them as categorically Lamarckian, a separate alternative to natural selection that did not mingle with it.

Ernst Mayr also presented Darwin’s thinking about use and disuse as singularly Lamarckian, in support of which he quoted from Origin of Species (1859: 134):

There can be little doubt that use in our domestic animals strengthens and enlarges certain parts and disuse diminishes them; and that such modifications are inherited.

Underscoring his Lamarckian take on Darwin, Mayr adds (1982: 691):

Use and disuse, of course, is of importance only if one believes in an inheritance of acquired characters. This Darwin affirms repeatedly … Darwin is quite positive: “Modifications [caused by use and disuse] are inherited.”

Standing alone, the sentence Mayr quotes from Origin of Species looks like a Lamarckian match. With each step back to see it in context, the resemblance fades.

In the next sentence, Darwin (1859: 134) refers to “… the effects of long-continued use and disuse,” not one generation to the next.

In the same paragraph he places use and disuse in the situation of stable selection pressures, offering as examples the “… wingless condition of several birds, which … inhabited several oceanic islands tenanted by no beasts of prey.”

On the next page he explicitly rejects Lamarckian inheritance of mutilations.

On the following page he clarifies “long-continued,” referring to “thousands of successive generations.”

And throughout Origin of Species, Darwin uses “acquired” only in reference to species across many generations in the context of specific selection pressures, not in the Lamarckian sense of individuals transmitting from one generation to the next characteristics acquired during their lifetimes.

In context, the “domestic animals” Darwin drew to our attention were domesticated species, not his neighbor’s individual dogs. Darwin saw species acquiring traits that became heritable when long-continued activities shaped selection pressures.

Jean Gayon repeated Mayr’s Lamarckian misreading of the identical quote from Origin of Species a decade later (1998 [1992]: 150).

Gayon is in the good company of many besides Huxley and Mayr. Science educators bemoan their failure to convince students that natural selection “does not involve effort, trying, or wanting” or “organisms trying to adapt” (Understanding Evolution, 2014). When their students accurately intuit that evolution has produced animals capable of effortful adaptation and these efforts can affect selection processes, this is considered “a significant departure from a scientific understanding of how animals change via natural selection” (Kelemen 2012: 71).

Huxley, Mayr, Gayon and science teachers stumbled over that ordinary and useful habit of thought, categorizing, while overlooking Darwin’s earnest doubts about the categories of his cultural inheritance (Beer 2009: xxx). The terms use and disusegrew into their common biological usage during the Lamarckian half-century that preceded Origin of Species. While Darwin was growing up, they acquired conceptual, social and political significance beyond concrete reference to specific animal activities. For many, the terms were synonymous with Lamarckian inheritance. Lamarckism has been called use-disuse theory.

When Darwin used these terms, he knew the importance of their secondary meanings for his readers. He also recognized the scientific and public relations merits of using these familiar terms for animal behavior in a more descriptive, pared down way.

Scientifically, he advanced more modest claims of animal agency than Lamarckian use of the terms. Darwin’s descriptive use of use and disuse created conceptual space for a developmental view of evolution that was not Lamarckian.

At the same time, Darwin wanted his readers to follow his argument and not give up on it. Pushing against the constraints of traditional terms by using them in nontraditional ways, Darwin’s “generous semantic practice” (Beer 2009: 33) allowed the reader to adjust their own yoke to the terms use and disuse. From his calibrated ambiguity, readers could hear in the text such Lamarckian overtones as their sensibilities favored.

Darwin’s semantic generosity quickened after publication of Origin of Species, as he responded to waves of criticism with a strategic retreat toward inclusiveness. In Variations of Animals and Plants under Domestication (1868), “anything which had been documented and accepted by a fellow scientist was included and assessed” (Vorzimmer 1963: 386). Darwin admitted for discussion a provisional hypothesis of Lamarckian inheritance that he had carefully avoided in Origin of Species. Darlington (1959: 41) complained that during this time “ambiguity … became the mode and standard of Darwin’s expression … which in the end soothed and satisfied the troubled world.”

As he changed successive editions of Origin of Species – to his wife Emma’s delight, adding “the Creator” in the second edition – Darwin remained committed to respectful, empirical inquiry that doubled as good public relations for his theory.

Bufflehead_taking_off
Bufflehead, Morro Bay State Park CA. by Kevin Cole 2008. http://commons.wikimedia.org/wiki/File:Male_Bufflehead_taking_off.jpg

While molecules eclipsed the behavior and development of whole organisms in 20th century evolutionary thought, accounts from Darwin’s vantage point persisted. Nobel physicist Erwin Schrödinger (1944: 113) echoed Darwin most clearly.

You simply cannot possess clever hands without using them for obtaining your aims… You cannot have efficient wings without attempting to fly… Selection would be powerless in ‘producing’ a new organ if selection were not aided all along by the organism’s making appropriate use of it….

Joining Huxley at Chicago’s centennial celebration of Origin of Species, Conrad Waddington (1959: 1636) presented a model of evolution that included animal choices.

Thus the animal by its behavior contributes in a most important way to determining the nature and intensity of the selective pressures which will be exerted on it.

Half a century on, Renée Duckworth (2009: 514) marked Origin’s sesquicentennial by reminding us that:

Changes in either the environment or an organism’s behavior can alter selection pressure. This places behavioral change on an equal footing with environmental change as a potential cause of evolutionary change … but despite the intuitive appeal of this idea, it remains largely unacknowledged in current evolutionary theory.

And Mary Jane West-Eberhard (2008: 902) rendered Darwin in contemporary terminology.

Much of Darwin’s discussion of … “use and disuse” refers not to Lamarckian inheritance but to what we would now call “phenotypic plasticity” [flexibility of the whole organism].

References

Beer, G. (2009). Darwin’s Plots (3rd ed.). Cambridge: Cambridge University Press.

Darlington, C. D. (1959). Darwin’s Place in History. Oxford: Basil Blackwell.

Darwin C. (1859) On the Origin of Species. In J. van Wyhe, ed. (2002), The Complete Work of Charles Darwin Online (http://darwin-online.org.uk).

Darwin, C. (1868). Variation of Animals and Plants Under Domestication. In J. van Wyhe, ed. (2002), The Complete Work of Charles Darwin Online (http://darwin-online.org.uk).

Duckworth, R. (2009). The role of behavior in evolution: A search for mechanism. Evolutionary Ecology 23: 513–531.

Gayon, J. (1992) [1998]. Darwin’s Struggle for Survival. Cambridge: Cambridge University Press.

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Tom Clark

As a psychologist, I have been interested in the role of behavior in evolution since my graduate training at the University of South Florida.

 

 

© 2015, Thomas L. Clark. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author(s) and source are credited. The statements and opinions expressed in this article are those of the author(s) and do not constitute official statements or positions of the Editors and others associated with SCIENCE DIALOGUES.

 


Darwin’s use of “use” and “disuse” (Part 1)

Tom Clark


Please note: this commentary, recovered on 8-Jan-2017, was originally published by the author, Tom Clark, on Science Dialogues on 28-Feb-2015.


LIKE OTHER NATURALISTS OF HIS DAY, Darwin thought that when animals used their bodies in some ways and not others, doing this and not that, these activities affected the evolution of their kind. Insect wings and rodent eyes became larger or smaller, more useful or less, depending on their ancestors’ use or disuse of their wings and eyes.

Unlike his peers, Darwin imagined animal behavior influencing evolution without Lamarckian inheritance of acquired characteristics. His most important discovery, natural selection, allowed him an alternative. Instead of direct transmission, from one generation to the next, of changes brought about by an animal’s activity within its lifetime, Darwin saw that such activity affects both how animals grow into adults—variation—and how natural selection plays out. And by way of long continued selection outcomes, characteristics expressed while growing up—specific variants—can become, somehow, more likely to develop in later generations. Hence, evolution.

Stretching to browse on trees did not cause giraffe ancestors to have offspring with longer necks. Rather, giraffe ancestors’ browsing habits swayed selection so giraffes that grew longer necks tended to have more offspring.

Giraffa_camelopardalis (5)
Photograph of Giraffa camelopardalis by Scott Harrison, Kruger Park 2006. http://commons.wikimedia.org/wiki/File:Giraffa_camelopardalis.JPG#file

Growing up mattered. Darwin observed variation among whole animals through their lifetimes, not variation among genes. Anything that made a growing child “not absolutely similar to the parent” was a source of variation that could make a difference in selection processes and outcomes (Darwin 1857). Darwin’s view was developmental, not Lamarckian.

Darwin understood that separating variation and selection was tidier in theory than in actual lives-in-progress. He took up his discussion of use and disuse in a chapter called “Laws of Variation” with a subheading “Use and disuse, combined with natural selection” (Darwin 1859: 131, italics added). What animals did with whom was a central and natural aspect of selection, as well as a source of variation. Animal behavior comprised and induced variation that was grist for selection and also part of the mill.

So he shows us in Origin of Species (1859: 136–143) that “the wings of some of the insects have been enlarged, and the wings of others have been reduced by natural selection aided by use and disuse.”

The wingless condition of so many Madeira beetles is mainly due to the action of natural selection, but combined probably with disuse.

And,

The eyes of some burrowing rodents are rudimentary in size… probably due to gradual reduction from disuse, but aided perhaps by natural selection . . . natural selection would constantly aid the effects of disuse.

So,

On the whole, I think we may conclude that habit, use, and disuse, have, in some cases, played a considerable part in the modification . . . of various organs; but that the effects of use and disuse have often been largely combined with, and sometimes overmastered by, the natural selection of innate differences.

Animals were protagonists in Darwin’s evolutionary plots. Theirs was an unwitting participation, animal intentions being of evolution, not about evolution. Still, animals’ semi-autonomous activities affected the evolution of their own kind and of others who came to their attention. Darwin saw, for example, that arbitrary “aesthetic” preferences of pollinating insects—going to these flowers more than those—affected selection of the flowers and of the insect’s nose, used to reach that flower’s nectar.

Darwin concerned himself with mechanisms of biological inheritance but had limited evidence to go on. Mendel published his experiments on plant hybridization in 1865 but with just three citations in 35 years, they never came to Darwin’s attention. Though he eventually proposed a Lamarckian mechanism of inheritance in his “provisional” hypothesis of pangenesis, Darwin continued to view the role of animal behavior in evolution as more developmental than Lamarckian. Animal activity naturally “either checked or favored” selection (1868: 234).

His developmental view of evolution endured August Weismann discerning a “barrier” between somatic and germ cells. Weismann’s famous barrier, allowing transmission of only germ cells to the next generation, was the death knell for Lamarckism. Yet Weismann affirmed Darwin’s view that “use and disuse” affected evolution by way of natural selection.

Weismann contrasted “mere disuse” with its consequence that “natural selection ceases to act” (1889: 15–16). By this relaxation of selection, disuse induced evolutionary change. Regarding use,

. . .  the direct influence of increased use during the course of a single life [cannot] produce hereditary effects without the assistance of natural selection (1889: 91).

And with the assistance of natural selection, it can.

. . . the use and disuse of parts can have no direct share in the process. . . . The fact, however, that we deny the transmission of the effects of use and disuse, does not imply that these factors are of no importance. . . . both use and disuse may lead indirectly to variations . . .  [that change selection processes and outcomes] (Weismann 1893: 395–396).

Darwin’s developmental view fell to the margins of evolutionary thought with the rediscovery of Mendel’s experiments that began the 20th century and initiated its turn toward a molecular gaze. In an historic cultural shift dubbed “bath-waterism” (Ewer 1960: 162), evolutionary thought threw out, along with the bath water of Lamarckism, the whole organism as an agent of evolutionary change. Evolutionary science transformed our image of ourselves from protagonists in the story of life to products of natural laws and chance, from the result of ancestors’ doings to the result of chemical happenings.

Our story changed from processes of selection that naturally had the benefit of vision and other senses and capabilities for the past 600 million years to “blind” selection the whole way; from an understanding that manners maketh the man, and action maketh the organism, to an understanding that tiny entities inside us make us who we are; from a story at the scale of organisms and lifetimes to a story about molecules across eons; from a story that includes growing up to a story that moves from one adult generation to the next by incantations of genes, environments and their so-called “interactions” (genes, of course, interact only with intra-cellular environments); from plot without humans to humans without plot; from a story teeming with human agency and meaning to a story of eggs regarding chickens as merely a way to make more eggs; from a story that tells us of life’s expanding autonomy, so what we do matters, to a story that tells us choice is a comforting illusion so we have no say in the course nature takes.

Among the ideas slanting these images of ourselves has been a misreading of Darwin’s use of use and disuse as simply Lamarckian.

References

Darwin, C. (1857). Letter to Asa Gray, 5 Sept. http://www.darwinproject.ac.uk/entry-2136.

Darwin C. (1859). On the Origin of Species. In J. van Wyhe, ed., (2002), The Complete Work of Charles Darwin Online (http://darwin-online.org.uk).

Darwin, C. (1868). Variation of Animals and Plants under Domestication. In J. van Wyhe, ed., (2002), The Complete Work of Charles Darwin Online (http://darwin-online.org.uk).

Ewer, R. F. 1960 Natural selection and neoteny. Acta Biotheoretica13:161-184.

Weismann, A. (1889). Essays Upon Heredity. Oxford: Clarendon Press.

Weismann, A. (1893). The Germ Plasm. New York: Scribner.


Tom Clark

As a psychologist, I have been interested in the role of behavior in evolution since my graduate training at the University of South Florida.

 

 

© 2015, Thomas L. Clark. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author(s) and source are credited. The statements and opinions expressed in this article are those of the author(s) and do not constitute official statements or positions of the Editors and others associated with SCIENCE DIALOGUES.