Notes on Fitness, Evolution, and Behavior

Fitness and Reproductive Success

  • Darwinian phrase: survival of the fittest is misleading if read as survival alone. In biology, fitness = reproductive success; long life without reproduction yields evolutionary failure because genes die with the bearer. The key criterion is reproduction.
  • Fitness in the modern sense: reproductive success is the measure of evolutionary success; what matters is how many offspring (and their offspring) an individual leaves behind.
  • Three-part core of natural selection (in modern terms):
    • Variations in reproductive success exist among members of populations.
    • These variations are partly due to genetic differences and are heritable.
    • These facts explain how gene pools and phenotypes evolve toward better adaptation.
  • Fitness can be quantified and applied to specific genes or whole organisms. For example, in fruit flies, single-gene changes can alter male courtship and thus fitness; experiments can predict how fast such alleles spread or are eliminated across generations.
  • Relative fitness and population context:
    • A numerical fitness value is usually relative to a population and environment, with the top genotype often set to 1.0, and others scaled relative to it.
    • Example framework: a mutant type raising three offspring might be assigned fitness 1.0; a competing type’s fitness could be 0.67 in that context (illustrative).
  • Fitness of behavior and optimality:
    • Behavior can be viewed as an evolved design to maximize fitness (i.e., reproductive success), but optimality is context-dependent and can vary with life stage and environment.
    • There exists an optimal level of a trait (e.g., aggression) that maximizes reproductive success; deviations in either direction (too little or too much aggression) reduce fitness.
  • Wynne-Edwards's challenge (group selection):
    • He argued that natural selection could favor reproductive restraint to prevent resource exhaustion and population crashes, proposing group-level selection (interdemic selection) as a mechanism.
    • The idea: groups with restraint outcompete groups without restraint.
    • Critics argued such group-level processes are implausible given gene flow, population structure, and lack of consistent empirical support for strict group selection dynamics.
  • Lack’s response and the Lack effect (clutch size):
    • David Lack argued that breeding restraint is largely illusory; the most productive clutch size is often the most common one thanks to natural selection optimizing reproductive output across the population.
    • The Lack effect (Figure 2-1): most common clutch size is typically the most productive, though not always; large broods can be more or less successful depending on year quality and parental condition.
    • Three contributing explanations for why the most common clutch size may be less than the most productive:
    • Resource and environmental variability allow better-conditioned individuals to raise larger broods; rare cases show larger clutches can outperform typical ones.
    • Conservation of parental resources: maximizing lifetime reproductive success may favor not exhausting the parent.
    • Measurement and long-term fitness: larger broods may have higher fledging numbers but lower adult survival or future breeding probability; hence a big brood does not necessarily equate to higher future gene propagation.
    • Overall: reproduction is often maximized by natural selection; the clutch size concept extends to other taxa and supports the idea that typical behavior is fit behavior; the trade-off between intensive care and fertility will be analyzed further in later chapters.
  • Hamilton’s inclusive fitness (the evolution of altruism):
    • Beyond personal reproduction, a gene can increase its representation by helping relatives who share copies of it (kin selection).
    • Inclusive fitness combines an individual’s own reproductive success with the impact of its actions on the reproduction of kin, weighted by relatedness.
    • Relatedness (r) and altruism: a cost (c) to the actor is offset by a benefit (b) to the recipient times the relatedness r. Hamilton’s condition for altruism to spread: c < r b \quad \text{(often written as } r b > c \text{)}
    • Example with sister vs cousin:
    • If the altruist helps a full sister (r = 0.5), the benefit to the sister is weighted by 0.5; the altruist gains if the resulting benefit to the sister (b) / 2 exceeds the cost (c).
    • If the recipient is a cousin (r = 0.125), the required benefit is much greater (or the cost much smaller) for altruism to be favored.
    • Classical result: inclusive fitness expands the scope of adaptation beyond personal reproduction to include kin-based effects.
    • The term inclusive fitness is often used interchangeably with kin selection, though there is some debate about terminology and levels of selection.
    • The broader implication: selection favors traits that maximize the replication of genes, whether via direct reproduction or via aiding kin who share those genes.
    • The policy implications: inclusive fitness reshapes how we view altruistic acts observed in nature (e.g., sterile workers, alarm calls) as consistent with evolution by natural selection when viewed through the kin-related benefits.
  • Levels of selection and debate:
    • Contenders include gene-level selection (the unit of selection), individual-level selection, and group-level selection.
    • Hamilton’s inclusive fitness and Lack’s work emphasize individual-level adaptation rather than species- or group-level selection as the primary driver.
    • Some resurgence of group-selection models exists, but the prevailing view emphasizes adaptation at the level of individuals (via kin selection) as the main explanatory framework.
    • Intragenomic conflict: sometimes genes within a single genome have conflicting interests; such conflicts are an area of ongoing study.
  • Heritability and the genotype-phenotype link:
    • Selection acts on phenotypes, but phenotypes reflect underlying genotypes; evolution occurs through changes in gene pools due to differential survival and reproduction.
    • Heritability is the proportion of phenotypic variance that can be attributed to genetic variance within a population and environment.
    • Heritability is population- and environment-specific; high heritability does not imply immutability under environmental change, and low heritability does not preclude genetic change under selection.
    • Classical example: egg production in hens shows higher heritability for egg size than for egg number: egg size responds better to selective breeding than egg number because of additive genetic variance present for size but not for number (in the studied population).
    • Formal definition (typical): h^2 = \frac{VA}{VP} where $VA$ is additive genetic variance and $VP$ is phenotypic variance. Heritability depends on both genotype variation and environmental variation in the population studied.
    • There are caveats to the concept: heritability is not a universal property of a trait; it can shift with changes in allele frequencies and environmental conditions; high heritability does not guarantee that a trait cannot be altered by environment or selection.
    • The egg example: egg number showed low heritability in one population but could be highly heritable in another population under different selective histories; likewise, selection experiments that deplete genetic variation for a trait reduce heritability estimates for that trait.
  • Natural selection and competition (intra- and interspecific):
    • Selection involves competition between genotypes within a population; it also acts as an ecological filter among species via competitive interactions and resource use.
    • Intraspecific competition: genotypes with higher reproductive success increase their representation in the next generation, changing the gene pool.
    • Interspecific competition: competition between species (e.g., starlings vs bluebirds) can indirectly drive evolutionary change in competing species through altered resource access or nest-site availability, even if there is no direct genetic competition between species.
    • Case study: starlings in North America, introduced in the late 19th century, became highly aggressive nest-site competitors, displacing other hole-nesting species. While starlings did not directly select for specific flicker genotypes, they acted as a selective pressure that could influence flicker populations via differential survival and reproduction.
    • The broader point: competition often manifests as differential success over limited resources, and natural selection can be understood as the cumulative outcome of such differential success over generations.
  • The animal as a strategist (metaphorical framing):
    • Organisms can be viewed as strategists designed by natural selection to maximize inclusive fitness, even though they do not consciously deliberate.
    • The metaphor helps explain functional significance of behaviors without implying intentional decision-making.
    • Example: a male Hamadryas baboon herds his harem to secure paternity and control over mates; however, other strategies (e.g., altruism or group-oriented behaviors) may be advantageous under different conditions, and natural selection tends to favor the strategy that maximizes fitness given the ecological context.

The Three-Part Statement of Natural Selection (revisited)

  • Summary of the mechanism:
    • There are variations in reproductive success among individuals.
    • These variations have a genetic basis and are heritable.
    • The differential reproductive success changes allele frequencies in the population, leading to adaptation over generations.
  • The role of environment and context:
    • Fitness values are relative to competing alternatives and the environment; a gene’s fitness can change across populations and over time.
    • The same gene can have different fitness effects depending on surrounding genetic background and ecological context.

Wynne-Edwards vs. Lack: Reproductive Restraint and Its Critics

  • Wynne-Edwards’s proposition: population-level restraint can evolve to prevent resource depletion and population crashes; group selection could account for this trait.
  • Major criticisms: typically, populations are not genetically isolated into groups with the required structure; genetic drift, gene flow, and lack of consistent data undermine its general applicability.
  • Lack’s empirical challenge and the Lack effect (Figure 2-1):
    • The most common clutch size is often the most productive, but not always; the most productive clutch size can be larger than the typical one in favorable conditions.
    • Three main explanations for the discrepancy:
    • Food availability and parental condition allow some individuals to raise larger broods; rare cases show larger broods achieving higher fledging success.
    • The parental resource constraint argument: effort in one year may reduce survival or future reproduction; the optimal strategy may be to not exhaust resources.
    • Measurement and interpretation issues: larger broods can reduce the weight or future reproductive prospects of offspring, complicating the measure of fitness.
    • Overall: Lack’s work supports the view that reproduction is, in many cases, maximized rather than restrained by natural selection, and that the most common reproductive strategy tends to be the most successful in typical conditions.
  • Implications for evolutionary theory:
    • The Lack effect supports the idea that fitness is best measured as the number of offspring that survive to reproduce, not simply the total number produced.
    • The relationship between clutch size and long-term fitness involves trade-offs among current reproduction, parental stamina, and future reproductive potential.

Hamilton’s Inclusive Fitness: A Quantitative Expansion

  • Inclusive fitness extends fitness to include kin-based effects, weighted by relatedness (r).
  • Core definition: inclusive fitness equals an individual’s own reproductive success plus the cumulative effects of its actions on the reproductive success of kin, weighted by relatedness.
  • Kinship and altruism (the classic thought experiment): an altruistic allele costs c to the actor and confers a benefit b to the recipient; the condition for such an allele to spread becomes c < r b .
  • Example calculations:
    • If you incur a cost c to help a full sister (r = 0.5) and the benefit to the sister is b, you gain if b/2 > c.
    • If the recipient is a cousin (r = 0.125), the required benefit is B such that B/8 > c (i.e., a much larger benefit or much smaller cost is needed).
  • Conceptual implications:
    • Inclusive fitness replaces a narrow focus on personal reproduction with a broader view that includes kin-directed effects on gene replication.
    • It helps explain altruistic behaviors that appear costly to the actor but increase the gene representation in the population when kin copies share the gene.
    • The idea also helps resolve classic altruism paradoxes (e.g., sterile worker behavior, alarm calls) by showing how gene-level advantages through kin support can drive such behaviors.
  • Levels of selection and the unit of analysis:
    • Kin selection is sometimes described as an intermediate between individual and group selection, but the authors prefer to avoid the term to prevent conflation of levels.
    • The central claim remains that natural selection operates most clearly and usefully at the level of the individual organism, via inclusive fitness, rather than at the group level.
  • Implications for understanding adaptation:
    • Kin selection explains why individuals can incur costs to aid relatives, because those relatives share copies of the altruistic gene.
    • Intrav genomic conflict remains a potential exception: some genes within an individual may maximize their own fitness at the expense of others.

Levels of Selection and Kin Selection (Clarifications)

  • The gene as the unit of selection: selection acts on replicators (genes) and their ability to propagate through generations; the organism’s phenotype and behavior are the vehicle by which genes achieve replication.
  • The argument that selection operates at multiple levels: while gene- and kin-level explanations are powerful, the practical and predictive framework for many behavioral and evolutionary questions remains anchored at the level of the organism (via inclusive fitness).
  • Dawkins’s “Selfish Gene” view (noting a shift in emphasis): the rhetoric of the gene as the unit of selection has influenced how we describe adaptation, but we still observe and study behavior at the level of the organism.
  • Intragenomic conflict as a potential exception: some genes may maximize their own transmission at the cost of others within the same genome, suggesting that selection dynamics can be more complex than a single unitary story.

Heritability: How Much of Variation Is Genetic?

  • Fundamental point: Selection acts on phenotypes, but evolution depends on genotypic variation that underlies those phenotypes.
  • Heritability definition: the proportion of observed phenotypic variance that can be attributed to genetic variance in a given population and environment. Formally, a common representation is h^2 = \frac{VA}{VP} where $VA$ is additive genetic variance and $VP$ is phenotypic variance.
  • Population and environment dependence:
    • Heritability is not a fixed property of a trait; it depends on the specific population and the environment under study.
    • A population with little genetic variance for a trait will show low heritability even if the trait is genetically influenced in other populations.
    • Environmental changes can alter V_P and thereby shift heritability estimates; a trait with high heritability in one environment might show lower heritability in another.
  • Egg size vs. egg number example (hens):
    • Egg size tends to be highly heritable (genetic variation in size is present and responds to selection).
    • Egg number often shows lower heritability in the same population because genetic variation related to reproduction rate is limited or interacts strongly with the environment.
    • Artificial selection experiments separating large-egg and small-egg lines show robust responses for egg size but not for egg number, illustrating how heritability shapes evolutionary potential.
  • Graphical illustration (Figure 2-3):
    • A hypothetical plot shows low heritability for egg number across a population and high heritability for egg size, with artificial selection separating lines by trait.
  • Practical implications:
    • Heritability estimates guide expectations about the pace and direction of evolutionary change under selection.
    • High heritability implies that selection can produce rapid genetic change; low heritability suggests environmental or non-additive genetic factors govern trait variation.
  • Important caveats about heritability:
    • High heritability does not imply immutability or inevitability of genetic change in response to selection or environment.
    • Heritability estimates are descriptive of current populations and conditions, not universal laws.

Natural Selection and Competition: Intra- and Interspecific

  • Core idea: Evolution via natural selection is driven by competition among genotypes within a population, altering the gene pool over generations. Interactions between species also shape evolutionary trajectories but do not, by themselves, cause a species to evolve.
  • Case example: starlings in North America
    • Starlings were introduced and rapidly became abundant; their aggressive nest-site competition displaced several other hole-nesting species (e.g., flickers, bluebirds).
    • Direct competition among species can influence which genotypes are favored by changing resource availability and habitat structure, thereby acting as a selective agent on populations that respond to those pressures.
    • The starling’s success is not a direct competition of one species against another at the genetic level, but a form of ecological competition that shapes which genotypes within other species are favored.
  • Direct vs indirect competition semantics:
    • Competition is often defined in terms of scarce resources and differential success, but it does not always require direct encounters or fights; resource limitation and ecological interactions suffice to create selective pressures.
    • The term competition can be used broadly in population biology to describe any scenario where individuals differ in reproductive success due to resource use or other constraints.
  • Summary takeaway:
    • Evolution by natural selection arises from intraspecific competition for resources, not from the existence of groups or species as deliberate units of selection. Ecological interactions between species can influence evolutionary outcomes, but the primary engine remains differential reproduction among individuals and their genes.

Summary of Key Concepts

  • Fitness (modern): reproductive success; not simply survival.
  • Three-part foundation of natural selection: variation in reproductive success, heritability, and evolution of gene pools toward adaptation.
  • Fitness is context-dependent and relative to alternatives; numerical values are often scaled with the fittest set to 1.0.
  • The Lack effect: typical clutch sizes often maximize reproductive success; environmental and resource constraints shape optimal strategies; absolute maximum reproduction is not always realized due to trade-offs.
  • Wynne-Edwards’s group selection vs. Lack’s individual-level perspective; empirical challenges to group selection as a universal mechanism.
  • Inclusive fitness (Hamilton): personal reproduction plus influence on kin’s reproduction, weighted by relatedness; altruism can evolve if c < r b
  • Kin selection and levels of selection: ongoing debate about the appropriate level of analysis, with emphasis on individuals and genes as primary units of adaptation; intragenomic conflict as a potential caveat.
  • Heritability: population- and environment-specific measure of the genetic contribution to phenotypic variance; simple to complex trait predictability depends on additive genetic variance and environmental context; illustrated by egg size (high heritability) vs. egg number (low heritability).
  • Natural selection and competition: competition within populations drives evolutionary change; interspecific competition can shape selection pressures indirectly; direct group-level selection remains controversial.
  • The animal as a strategist: convenient metaphor for understanding behavior as evolved strategies to maximize inclusive fitness, while recognizing that animals do not consciously plan their actions.

Suggested Readings (as listed in the transcript)

  • Dawkins, R. 1976. The selfish gene. London: Oxford University Press.
  • Dawkins, R. 1982. An agony in five fits. Chapter 10 of The extended phenotype. Oxford: W. H. Freeman.
  • Williams, G. C. 1966. Adaptation and natural selection. Princeton: Princeton University Press.

The Animal as Strategist (closing note)

  • Organisms can be viewed as devices optimized by natural selection to replicate their genes.
  • The metaphor of strategy helps discuss the functional significance of behavior without implying conscious decision-making.
  • An example: a male Hamadryas baboon herds his females to secure reproductive access and fidelity, illustrating how behavior aligns with maximizing inclusive fitness.