Levels of Selection
Lukas Schärer
Evolutionary Biology
Zoological Institute
University of Basel

118.9.2024

Advanced-level Evolutionary Biology

Fictional self-assembly2

a clip from the Hollywood movie Terminator 2: the T-1000 self-assembles

Actual self-assembly3

a clip from an MDR nature documentary: slime mold cells self-assemble

Summary: levels of selection• levels of selection• building higher levels• a levels of selection view of the world• genomic con ict• group selection

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Levels of selection• “I am pretending to a unity, deep inside myself, I know does notexist. I am fundamentally mixed, male with female, parent withoffspring, warring segments of chromosomes that interlocked in
strife millions of years ... (ago).”W. D. Hamilton (in Narrow Roads of Gene Land, 1997)

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Levels of selection• genes ➝ cells ➝ individuals ➝ kin ➝ groups ➝ species

6from Stearns & Hoekstra 2005

Levels of selection• uncritical ‘group selectionist’ arguments were the norm in thescienti c literature before the 1970s• ‘frogs lay so many eggs to ensure the survival of the species, because tadpoles
suffer extremely high rates of predation’• ‘wolves have ritualised displays and combats, because escalated combats would
be too disadvantageous for the survival of the species’• such arguments were pervasive in old nature documentaries, andthey remain common in the general press and the general public• but they are usually unfounded, with no clear evidence that such traits haveevolved to the bene t of the species• instead, such traits can be shown to be optimal for the individuals• and many traits are clearly maladaptive at the level of the species• group selection has been shown to work under speci c conditions• and there is an ongoing debate about how important group selection is7

see Reeve & Keller 1999

Levels of selection• Dawkins (1976) proposed the perspective of the sel sh gene as acounterpoint to the prevailing ‘group selectionist’ mind frame• by a ‘gene’ Dawkins means “any portion of chromosomal material that potentiallylasts for enough generations to serve as a unit of natural selection”• and Dawkins did not actually claim that the other levels were unimportant• replicators are the enduring units of replication (i.e. information)• replicators do not age (although the DNA ‘storage medium’ of course can)• vehicles are the phenotypic effects of the replicators (i.e. matter)• vehicles can age and they are actually dispensable• natural selection cannot pick directly among the different
replicators (i.e. the alleles of a gene)• instead natural selection picks among vehicles (i.e. the different
phenotypes created by the different alleles)• and the successful vehicles contain the (thereby) successful alleles (and also theother genes carried by the same vehicle)

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Building higher levels• a ‘heuristic’ model to help visualise
the possible interactions• repulsive forces• e.g. close spatial proximity between
vehicles leads to more resourcecompetition• attractive forces• e.g. a larger vehicle size allows to escapesome predation• centrifugal forces• e.g. the allure of a leaving the group andliving a ‘solitary’ existence• this may often no longer be possible, but
early in a level shift it likely was possible
9from Keller & Reeve 1999

Building higher levels• the inclusive tness concept in uences how easily co-operation
between vehicles can evolve• this can be captured by Hamilton’s rule, with the inequality b· r > c• b is tness bene t for the recipient of a co-operative act• c is tness cost for the helper of performing the co-operative act• r is relatedness of the recipient to the helper (i.e. a value between 0 and 1)• the larger the relatedness, the more easily the inequality is ful lled• many co-operative systems have mechanisms that ensure a high relatedness• co-operative problems can arise if relatedness is reduced• so co-operation more easily evolves between highly related vehicles(such as clonal cells within a body) than between relatively
unrelated vehicles (such as birds in a ock)

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Building higher levels• how can selection that acts among low-level vehicles favour theevolution of higher-level vehicles?
• how does selection at one level affect the selection at levels aboveand below that level?
• do the lower-level processes necessarily stop once a higher level
has emerged?

11A levels of selection view of the world• the origin of co-operating ‘replicator-level vehicles’ essentiallyrepresents the question about the origin of life
• the earliest forms may have been RNA molecules that had catalytic functions• life appears to be monophyletic (since all known life is based on DNA andRNA, using essentially the same genetic code)• the integration into higher-level vehicles may result from bene ts of• complementation (e.g. via the formation of ‘chromosomes’)• compartmentalisation (e.g. via the formation of cell walls)• division of labour (e.g. via formation of cell types in multicellular vehicles)• these early processes are dif cult to study• the environmental conditions are very different today• there originally was almost no oxygen in the atmosphere• there was a vast amount of time available• there were amazingly many different places and conditions on Earth• and we are not certain that life originated on Earth (panspermia)

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A levels of selection view of the world• increased complexity and function resulted from co-operation andfusion between lower-level vehicles• shift from pro- to eukaryotes (via acquisition of mitochondria and chloroplasts)• similar transitions are still occurring today in the context of symbiosis• the bene ts probably often result from complementation of functions• an active eld of research that greatly bene ts from genomics

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A levels of selection view of the world• shifts from uni- to multi-cellular organisation• occurred may times during evolution in many organismal groups• can still be observed today in a number of organismal groups (e.g. facultative
multi-cellularity in social bacteria, slime molds, volvocine green algae)• bene ts likely result from division of labour and large size
• but such shifts often also lead to problems with cheating• origin of the soma-germline distinction (i.e. the origin of death as a normal stepin the life history of an organism)

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Dictyostelium discoideum

Volvox sp.

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Myxobacterium xanthus

14A levels of selection view of the world• the slime mold, Dictyostelium discoideum• spends most time as a free-living haploid amoeboid cell that divides asexually• when starved 10’000 to 100’000 cells will aggregate into a ‘slug’• the anterior 20% of the slug differentiates into a stalk (‘soma’)• most of the remaining cells become spores that disperse (‘germ-line’)• this functional division leads to a potential for cheating

swarming to chemoattractant

crawling and stalk formation

15A levels of selection view of the world• in Dictyostelium discoideum the cells of different genetic clones canmix, but may not contribute equally to spore and stalk formation
prestalk region of slug

prespore region of slug

microsatellite genotypes of slugsformed from single clones andfrom mixed clones

relative contributions to (pre)sporesand (pre)stalks of mixed clones
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from Strassmann & al. 2000

mixtures of different (unlabelled)
clones with a GFP-labelled clone
reveals unequal distribution of theGFP-clone within the slugs
from Santorelli & al. 2008

A levels of selection view of the world• shifts from individual life to life in social groups• the frequent occurrence of eusociality in Hymenoptera may be linked to their
special genetic system (haplo-diploidy)• this causes the workers to be more closely related to their sisters than to theirown offspring

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Central American Paper Wasp (Apoica pallens) by Silas Kenta silly image of an anthill

A levels of selection view of the world• shifts from individual life to life in social groups• part-time social groups of (generally) unrelated individuals are formed during
sexual reproduction• relatedness, r is usually low between the parents (that is kind of the point of sex)
• r is relatively high among the offspring, and also between the parents and theoffspring (but this may depend on the level of multiple paternity)• the centrifugal forces are high because there may be other mating opportunities
for both parents (which can lead to strong con icts between male and female)

male, nest and female of the Collared Flycatcher (Ficedula albicollis)

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A levels of selection view of the world• depending on your speci c research question, a levels of selection
view may not necessarily be needed• but you should decide this only after careful consideration and keep
this possibility in the back of your mind
• ask yourself the following questions:• at which level is selection likely acting in a given interaction?
• could there be con icts of interest between different levels of selection?
• which vehicle (i.e. gene, cell, mating partner) bene ts from a given outcome?
• how labile is a system? can its components function independently?
• which traits of a given system could potentially be adaptations that enforce cooperation (i.e. policing)?

• sometimes the con icts between levels of selection can be dif cultto detect due to a balance of power• they often only become evident when two individuals from diverged populations
are crossed
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Genomic con ict• selection can favour a trait at one level but
select against it at another level• imagine a scenario where carrying bothmitochondria of type A and type a isadvantageous at the higher level, the cells• then a selection process (b) or a biased
segregation (c) occurring at the lowerlevel, the organelles, can be detrimental to
the tness of the higher level

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from Stearns & Hoekstra 2005

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Genomic con ict: meiotic drive• mitosis and meiosis are generally expected to lead to a fairtransmission of the genetic material in the parental cells (or theparental individuals) to the daughter cells (or the offspring)• for example, during meiosis a heterozygous Aa individual is
expected to produce 50% A gametes and 50% a gametes (equalsegregation or fair meiosis)• but certain alleles have been shown to cause meiotic drive (andthus lead to segregation distortion)

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Genomic con ict: the t haplotype in mice
• three ‘alleles’ occur at the t complex: T, t and +• but the main effects can be explained by just considering t and +• genes in the t complex produce a toxic effect on + carrying sperm• spermatogenesis appears normal, but the + carrying sperm are non-functional• genes in the t complex also produce an antidote, which allows
normal function in the t carrying sperm• at the site of fertilisation, t/+ males exhibit 90-100% of t-carrying
sperm (while there is no apparent effect on the female gametes)• so at the level of the individual gamete, the t haplotype is clearly favoured• the t/t genotype is lethal, causing male-sterility or reduced viability• so at the level of the individual mouse, the + haplotype is clearly favoured• this does not lead to xation, but to a stable coexistence of t and +• it was estimated that the combination of observed tness effects of the t and +haplotypes, the expected frequency of t carrying mice should be about 70%

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Genomic con ict: meiotic drive• meiotic drive is probably rare
• usually it involves a system with a toxin and an antidote• this requires that the alleles are tightly linked (maybe one reason for theevolution of genetic recombination is to break such linkage)• it also requires that the toxin and antidote originate together (because alone
these alleles offer no advantage)• the processes of mitosis and meiosis might be expected to show
evidence for selection against segregation distortion

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mitosismeiosisGroup selection• selection may occur between groups of individuals, but• the groups need to have a considerable risk of extinction• the migration rate between groups needs to be rather low (or at least biased)

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Group selection: the t haplotype in mice revisited• earlier, I mentioned that the expected frequency of t carrying miceis about 70%, but the observed frequency is usually only 6-25%• could selection at the group level explain this difference?
• groups often contain only two resident males• so if the t haplotype increases in frequency within a group, bothresident males may become t/t and will thus die or be sterile• if the migration rates between groups are suf ciently low, then alack of (fertile) resident males could lead to group extinction,• the t haplotype carrying groups may thus go extinct more often• and they can then be recolonised from the productive groups thatlack t carrying individuals

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from Carroll & al. 2004

Group selection: t haplotype in mice revisited• this is a nice idea, but likely not true
• wild-type males (and females) can becompetitively superior• it is mainly selection at the individuallevel that maintains low t frequencies

from Carroll & al. 2004

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Summary: levels of selection• levels of selection• building higher levels• a levels of selection view of the world• genomic con ict• group selection

27Literature• Mandatory Reading• Reeve & Keller (1999). Levels of selection: burying the units-of-selection debateand unearthing the crucial new issues. Chapter 1 in Keller (ed). Levels ofSelection in Evolution. Princeton University Press.

• Suggested Reading• Pages 197-206 in Chapter 9 on ‘Genomic Con ict’ of Stearns & Hoekstra (2005).
Evolution: An Introduction. 2nd Edition. Oxford University Press.
• Okasha (2024). Cancer and the levels of selection. The British Journal for thePhilosophy of Science, 75: 537-560.

• Books• Dawkins (1976). The Sel sh Gene. Oxford University Press.

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