Module 8: Evolution & Colony Genetics
The evolution of eusociality in honeybees is one of the great puzzles of biology. How can natural selection favor workers that sacrifice their own reproduction? The answer lies in the interplay of haplodiploidy, kin selection, and the superorganism concept — where the colony, not the individual, is the unit of selection. Today, these ancient evolutionary strategies face modern threats: Varroa destructor, neonicotinoids, and habitat loss are driving global colony declines.
8.1 Haplodiploidy & Kin Selection
Haplodiploid Sex Determination
Honeybees, like all Hymenoptera (ants, bees, wasps), have a haplodiploidsex determination system. Fertilized eggs develop into diploid females (2n = 32 chromosomes), while unfertilized eggs develop into haploid males (drones, n = 16). This means:
Queen
Diploid female (2n = 32). Mated during a single mating flight period (1–3 flights over 1–2 days). Stores sperm in her spermatheca for her entire life (2–5 years). Can selectively fertilize eggs (worker/queen) or lay unfertilized eggs (drones).
Workers
Diploid females (2n = 32). Functionally sterile due to pheromonal suppression by the queen (queen mandibular pheromone inhibits ovary development). In queenless colonies, some workers can lay unfertilized eggs (producing only drones).
Drones
Haploid males (n = 16). Develop from unfertilized eggs via arrhenotokous parthenogenesis. Their only function is mating; they die during copulation (endophallus everts explosively, tearing from the abdomen). Drones have no father but have a grandfather.
Relatedness Coefficients
The key insight of haplodiploidy is that it creates asymmetric relatedness. Consider a queen mated to a single drone (monandry):
Sister-sister relatedness:
\[ r_{\text{sisters}} = \underbrace{\frac{1}{2}}_{\text{from mother}} + \underbrace{\frac{1}{2} \times \frac{1}{2}}_{\text{from father (haploid: all genes shared)}} \]
Wait — let's derive this more carefully. The father is haploid, so all his sperm are genetically identical. Every sister receives exactly the same paternal genome. From the mother (diploid), sisters share genes with probability 1/2 (standard Mendelian). Therefore:
\[ r_{\text{sisters}} = \frac{1}{2}\left(\frac{1}{2}\right) + \frac{1}{2}(1) = \frac{1}{4} + \frac{1}{2} = \frac{3}{4} \]
where the 1/2 prefactors account for the fraction of the genome inherited from each parent. Compare this with standard diploid relatedness:
\[ r_{\text{mother-daughter}} = \frac{1}{2} \qquad r_{\text{sister-sister (diploid)}} = \frac{1}{2} \]
Under haplodiploidy, a worker is more related to her sisters (\(r = 3/4\)) than she would be to her own daughters (\(r = 1/2\)). This creates a genetic incentive for workers to help raise sisters rather than produce their own offspring.
Hamilton's Rule
William Hamilton (1964) formalized the conditions for the evolution of altruistic behavior. An altruistic allele spreads when:
\[ rB > C \]
where \(r\) is the genetic relatedness between actor and beneficiary,\(B\) is the fitness benefit to the beneficiary, and \(C\) is the fitness cost to the actor. For a worker bee sacrificing reproduction to help raise sisters:
\[ \frac{3}{4} B > C \]
The condition is easily satisfied when \(B > \frac{4}{3}C\) — if helping produces more than 1.33 sisters per unit of own reproduction sacrificed, altruism is favored. In a well-functioning colony where workers are far more efficient at brood-rearing than solitary reproduction, this condition is readily met.
Inclusive Fitness Derivation
The inclusive fitness of an individual is the sum of its direct fitness (own reproduction) and indirect fitness (reproduction of relatives, weighted by relatedness):
\[ W_{\text{inclusive}} = W_{\text{direct}} + \sum_j r_j \cdot \Delta W_j \]
where the sum is over all relatives \(j\), \(r_j\) is the relatedness to relative \(j\), and \(\Delta W_j\) is the change in relative\(j\)'s fitness caused by the focal individual. For a worker bee:
\[ W_{\text{worker}} = \underbrace{0}_{\text{direct (sterile)}} + \underbrace{\frac{3}{4} \cdot n_{\text{sisters}}}_{\text{indirect via sisters}} + \underbrace{\frac{1}{4} \cdot n_{\text{brothers}}}_{\text{indirect via brothers}} \]
Note that workers are related to brothers by only \(r = 1/4\) (they share 1/2 of maternal genes but 0 paternal genes, since brothers develop from unfertilized eggs). This creates a conflict of interest over sex ratios: workers “prefer” a 3:1 female-to-male ratio (maximizing inclusive fitness), while the queen “prefers” 1:1 (Fisher's principle). Empirical data show that colonies tend toward the worker-optimal 3:1 ratio, indicating that workers exert some control over sex allocation.
Complications: Polyandry
The simple \(r = 3/4\) calculation assumes monandry (queen mated with one drone). In reality, queens mate with 12–20 drones, reducing average sister-sister relatedness to approximately \(r \approx 0.25\text{--}0.35\) (closer to the diploid value). This means haplodiploidy alone cannot fully explain eusociality — other factors (colony efficiency, ecological constraints on solitary reproduction, pre-existing parental care) are also important (Nowak, Tarnita & Wilson, 2010).
8.2 The Superorganism Concept
Hölldobler and Wilson (2009) formalized the concept of the colony as a superorganism — an entity where the colony, not the individual bee, is the unit upon which natural selection primarily acts. The analogy between a bee colony and a multicellular organism is remarkably precise:
Organism
- Germ cells (reproduce)
- Somatic cells (sterile, support)
- Immune system (defense)
- Nervous system (coordination)
- Circulatory system (nutrient distribution)
Superorganism (Colony)
- Queen + drones (reproduce)
- Workers (sterile, support)
- Guard bees (defense)
- Pheromone system (coordination)
- Trophallaxis (nutrient distribution)
Temporal Polyethism
Workers progress through a stereotyped sequence of tasks as they age, regulated by juvenile hormone (JH) titers:
Days 1–3: Cell cleaning — Young bees clean and polish brood cells. JH levels very low.
Days 3–12: Nursing — Feed larvae with royal jelly (from hypopharyngeal glands) and pollen. JH rising slowly.
Days 12–18: Wax building & food processing — Secrete wax, construct comb, process nectar into honey. JH at moderate levels.
Days 18–21: Guard duty — Inspect incoming bees at the entrance, challenge non-nestmates. JH rising.
Days 21+: Foraging — Collect nectar, pollen, propolis, and water. JH at peak levels. Most dangerous task — forager life expectancy is only ~7 days.
Optimal Caste Ratios
The colony-level fitness depends on the allocation of workers to different tasks. Let\(f_i\) be the fraction of workers assigned to task \(i\). Colony fitness can be modeled as a Cobb-Douglas production function:
\[ W_{\text{colony}} = A \prod_{i=1}^{k} f_i^{\alpha_i} \qquad\text{subject to}\quad \sum_i f_i = 1 \]
where \(\alpha_i\) represents the importance of task \(i\). Optimizing by Lagrange multipliers yields the optimal allocation:
\[ f_i^* = \frac{\alpha_i}{\sum_j \alpha_j} \]
Workers are allocated to each task in proportion to its importance. The response threshold model (Section 7.3) provides the mechanism by which individual bees, without knowing the optimal ratios, collectively achieve approximately optimal allocation through local stimulus-response rules.
8.3 Polyandry & Genetic Diversity
Honeybee queens are highly polyandrous, mating with 12–20 drones during 1–3 mating flights in the first 1–2 weeks of life. Mating occurs at drone congregation areas (DCAs)located 10–40 m above ground, where drones from many colonies gather. The queen stores ~5–6 million sperm in her spermatheca, sufficient for her entire reproductive life.
Genetic Diversity Within the Colony
With \(M\) mates contributing sperm in approximately equal proportions\(p_i \approx 1/M\), the intra-colony genetic diversity can be quantified using Simpson's diversity index:
\[ D = 1 - \sum_{i=1}^{M} p_i^2 \]
For equal paternity shares (\(p_i = 1/M\)):
\[ D = 1 - M \cdot \frac{1}{M^2} = 1 - \frac{1}{M} = \frac{M-1}{M} \]
For \(M = 15\) mates: \(D = 14/15 \approx 0.93\). This high diversity has multiple adaptive benefits confirmed by experimental studies:
Disease Resistance (Tarpy 2003; Seeley & Tarpy 2007)
Genetically diverse colonies are more resistant to brood diseases (American foulbrood, chalkbrood). Different patrilines have different disease susceptibilities, so epidemics are less likely to devastate the entire colony. Experimentally, colonies headed by multiply-mated queens had 2–5x lower disease prevalence than singly-mated controls.
Thermoregulatory Efficiency (Jones et al. 2004)
Different patrilines have different temperature response thresholds for fanning and shivering. This genetic variation broadens the colony's thermoregulatory capacity, reducing brood temperature variance by ~30% compared to monandrous colonies.
Behavioral Flexibility
Genetic variation in response thresholds for different tasks ensures that the colony can dynamically reallocate workers as demands change. Some patrilines are biased toward foraging; others toward defense or nursing. This genotypic task specialization improves colony-level efficiency.
Effective Mating Number
When paternity shares are unequal, the effective mating number captures the functional number of fathers:
\[ M_e = \frac{1}{\sum_{i=1}^{M} p_i^2} \]
If one drone sires 50% of offspring and 14 others share the remaining 50%,\(M_e \approx 3.6\) rather than the nominal 15. High effective mating number requires approximately equal sperm use from each drone — which is what is observed in practice (Haberl & Tautz, 2003), suggesting active sperm mixing in the spermatheca.
8.4 Colony Collapse Disorder & Varroa
Colony Collapse Disorder (CCD) emerged as a major concern in 2006–2007, when US beekeepers reported losing 30–90% of their colonies. The signature of CCD is the rapid disappearance of adult workers, leaving the queen, brood, and food stores behind. No single cause has been identified; rather, CCD appears to result from the interaction of multiple stressors.
Varroa destructor
The ectoparasitic mite Varroa destructor is widely considered the most important driver of global honeybee decline. Originally a parasite of the Asian honeybee (Apis cerana), it switched to Apis mellifera in the mid-20th century and has since spread worldwide (except Australia). Key biology:
Feeding: Ramsey et al. (2019) overturned decades of assumption by showing that Varroa feeds primarily on the fat body (the insect equivalent of liver + adipose tissue), not hemolymph. This impairs immune function, detoxification capacity, and overwinter survival.
Viral transmission: Varroa is the primary vector for deformed wing virus (DWV), a picorna-like RNA virus. Without Varroa, DWV exists as a low-titer covert infection; with Varroa, viral loads increase 100–1000x, causing overt disease (crumpled wings, shortened lifespan, impaired learning).
Reproduction: Female mites enter brood cells just before capping, preferring drone brood (longer development time allows more mite offspring). Each foundress produces 1–2 viable daughter mites per worker cell, 2–3 per drone cell.
Population Dynamics: Bee-Mite Coupled Equations
The interaction between bee and mite populations can be modeled as a predator-prey system:
\[ \frac{dB}{dt} = rB\left(1 - \frac{B}{K}\right) - \alpha BV \]
\[ \frac{dV}{dt} = \beta BV - \mu V \]
where:
- \(B\) = bee population, \(V\) = Varroa population
- \(r\) = bee intrinsic growth rate (~0.02/day in summer)
- \(K\) = carrying capacity (~40,000 bees)
- \(\alpha\) = mite virulence (bee death rate per mite per bee)
- \(\beta\) = mite reproduction rate (proportional to available brood)
- \(\mu\) = mite natural mortality rate
Without treatment, the mite population grows exponentially during the brood season, reaching a critical threshold (~3,000–5,000 mites per colony) at which DWV prevalence exceeds the colony's immune capacity, triggering collapse — typically in late autumn when the last generation of long-lived winter bees is raised with compromised fat bodies.
Neonicotinoid Sublethal Effects
Neonicotinoid insecticides (imidacloprid, clothianidin, thiamethoxam) are systemic pesticides that appear in nectar and pollen at sublethal concentrations (1–10 ppb). At these levels, they do not directly kill bees but impair critical behaviors:
Navigation Impairment
Fischer et al. (2014) showed that sublethal neonicotinoid exposure reduces waggle dance accuracy: direction error increases ~40%, distance encoding error increases ~30%. Homing success after displacement drops by 30–50% (Henry et al., 2012).
Learning & Memory
Neonicotinoids act on nicotinic acetylcholine receptors (nAChRs) in the mushroom bodies. Proboscis extension reflex (PER) conditioning shows 40–60% reduction in associative learning performance at field-relevant doses (Williamson & Wright, 2013).
The interaction between Varroa and neonicotinoids is synergistic: neonicotinoid-impaired immune function makes bees more susceptible to Varroa-vectored viruses, while Varroa-weakened bees are less able to detoxify pesticide residues (Doublet et al., 2015).
8.5 Haplodiploidy & Relatedness
Chromosome flow in a haplodiploid mating system. The queen (2n) mates with a haploid drone (n). Fertilized eggs become diploid workers/queens; unfertilized eggs become haploid drones. Relatedness coefficients are shown for each relationship.
8.6 Simulation: Hamilton's Rule, Varroa Dynamics & Genetic Diversity
Three-panel simulation: (1) Hamilton's rule parameter space showing when altruism is favored for different relatedness values, (2) bee-Varroa population dynamics with and without treatment, and (3) colony genetic diversity as a function of queen mating number.
Hamilton's Rule, Bee-Varroa Dynamics & Genetic Diversity
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References
- Hamilton, W. D. (1964). The genetical evolution of social behaviour. I & II. Journal of Theoretical Biology, 7(1), 1–52.
- Hölldobler, B., & Wilson, E. O. (2009). The Superorganism: The Beauty, Elegance, and Strangeness of Insect Societies. W. W. Norton & Company.
- Tarpy, D. R. (2003). Genetic diversity within honeybee colonies prevents severe infections and promotes colony growth. Proceedings of the Royal Society B, 270(1510), 99–103.
- Seeley, T. D., & Tarpy, D. R. (2007). Queen promiscuity lowers disease within honeybee colonies. Proceedings of the Royal Society B, 274(1606), 67–72.
- Ramsey, S. D., et al. (2019). Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph. Proceedings of the National Academy of Sciences, 116(5), 1792–1801.
- Nowak, M. A., Tarnita, C. E., & Wilson, E. O. (2010). The evolution of eusociality. Nature, 466(7310), 1057–1062.
- Henry, M., et al. (2012). A common pesticide decreases foraging success and survival in honey bees. Science, 336(6079), 348–350.
- Fischer, J., et al. (2014). Neonicotinoids interfere with specific components of navigation in honeybees. PLoS ONE, 9(3), e91364.
- Williamson, S. M., & Wright, G. A. (2013). Exposure to multiple cholinergic pesticides impairs olfactory learning and memory in honeybees. Journal of Experimental Biology, 216(10), 1799–1807.
- Doublet, V., et al. (2015). Bees under stress: Sublethal doses of a neonicotinoid pesticide and pathogens interact to elevate honey bee mortality across the life cycle. Environmental Microbiology, 17(4), 969–983.
- Jones, J. C., et al. (2004). Honey bee nest thermoregulation: Diversity promotes stability. Science, 305(5682), 402–404.
- Haberl, M., & Tautz, D. (2003). Sperm usage in honey bees. Behavioral Ecology and Sociobiology, 29(2), 113–118.