Animal Reproduction: Sex Role Reversal, Sperm Competition & Polyandry

Review of Traditional Sex Roles (connection to previous lecture)

• Historically—following Darwin & Bateman—sexual-selection theory assumed:
  • Males = competitive sex; females = choosy sex.
  • Rationale derived from anisogamy (size-based gamete dimorphism):
    • Female eggs = few, large, costly.
    • Male sperm = many, small, inexpensive.
• Consequences re-capped from yesterday:
  • Male reproductive success rises linearly with number of mates (Bateman gradient).
  • Female success plateaus after first, fully-fertilising mating.
• Limitations already flagged: species diversity → many deviations from this “default.”

Sex-Role Reversal

• Definition: situations in which males become choosy and females compete.
• Mechanistic trigger: when male parental investment becomes the limiting resource.
• Classic vertebrate examples
  • Seahorses & pipefishes (Syngnathidae):
    • Males carry embryos in a brood pouch ⇒ functional “male pregnancy.”
    • Gestation \approx several weeks; during that period males cannot remate, thus are the scarce sex.
    • Females display bright silver abdominal bands (pipefish) as ornaments to attract incubating males (Sarah Flanagan’s work).
• Empirical pattern (Flanagan heat map):
  • X-axis = number of bands; Y-axis = proportional abdominal area covered.
  • Hot colours (red/orange) = high female fitness.
  • Positive correlation → ornaments are honest signals of female condition.
• Mutual ornamentation
  • Crested auklets: both sexes exhibit forehead crests ⇒ mutual mate choice rather than strict reversal.
• Research bias acknowledged: historical focus on male traits; sex-role-reversed systems still understudied.

Post-Copulatory Sexual Selection: Sperm Competition

• Polyandry (females mating >1 male) means mating ≠ fertilisation.
• Females possess sperm-storage organs (e.g.
  • Insects: spermatheca).
  • Storage provides an arena for sperm competition—selection continues after copulation.
• Chronology of the idea:
  • Thought rare until Jeff Parker’s 1970s work on yellow dung flies → revealed polyandry nearly ubiquitous; revolutionised sexual-selection models.

Engaging in Sperm Competition (offensive tactics)

• Increase sperm number
  • Large testes ⇒ larger ejaculates.
  • Dung beetles with alternative tactics: small “sneaker” males lack horns but invest disproportionately in testes mass.
• Improve sperm quality
  • Rodent comparative study: polyandrous species evolve longer sperm; longer flagella ⇒ faster swimming.
• Strategic allocation
  • UWA cricket experiments (Thomas & Simmons):
    • Male ejaculates to females of differing mating histories.
    • Total sperm number: no significant adjustment.
    • Viability (%):
    – Unmated female ⇒ \approx 88\% live.
    – Female mated once ⇒ raises viability.
    – Female mated many times ⇒ sharp drop (resource saving when chance of success is low).
  • Mechanism detection: males use cuticular-hydrocarbon (CHC) scent signatures; ability to count number of distinct male odours on female.

Avoiding Sperm Competition (defensive tactics)

• Mate guarding
  • Persist near female post-mating; common in weapon-bearing species (e.g. giraffe weevils).
• Mating plugs / genital damage
  • Nephilengys spiders: male breaks pedipalp, physically sealing female.
• Biochemical manipulation
  • Drosophila seminal proteins ↓ female receptivity for \approx 48\,h—long enough for egg-laying, saving male time/energy.
• Sperm removal devices
  • Damselfly penis armed with barbed spines scrapes rival sperm (BBC footage).
    • Sequence: clasp, sperm translocation to secondary genitalia, scraping, own ejaculate deposition.

Continuum Diagram (engagement ↔ avoidance)

• Top (avoidance): mate guarding, plugs, receptivity-blocking proteins.
• Middle: mixed strategies (e.g. sperm removal, strategic viability).
• Bottom (engagement): larger testes, more sperm, faster sperm.

Cryptic Female Choice (post-copulatory female control)

• Females can differentially utilise or eject sperm after mating.
• Mechanisms: terminate copulation, destroy sperm, remove plugs, active sperm ejection (e.g. domestic chickens bias toward dominant males).
• Empirically difficult to separate from male-driven sperm competition; often requires elegant experimental design.

Polyandry: Adaptive Value for Females

• Revised Bateman gradient: evidence accumulating that female fitness also increases with additional matings; slope steeper than classical model.

Direct Benefits

• Fertility assurance: insufficient sperm from single male; multiple matings guarantee egg fertilisation.
• Nutritional gifts / nuptial feeding
  • Mormon cricket spermatophylax: bulky protein mass around sperm packet; multiple gifts ⇒ multiple egg clutches.
  • Dolomedes fishing spiders: males die post-copulation; cannibalism supplies nutrients → larger, healthier egg sacs.

Indirect (Genetic) Benefits

1. Diverse-genes hypothesis (colony/offspring heterogeneity)
   • Honeybees:
     • Queens mate with many drones in aerial swarms.
     • Genetically diverse colonies build comb faster, forage more, resist parasites better ⇒ winter survival.
2. Compatible-genes hypothesis
   • Sand lizards: females bias paternity toward males with maximally different MHC alleles → avoids inbreeding, enhances immune response.
   • Requires multiple matings + cryptic female choice, because compatibility only assessed post-copulation.
3. Good-genes vs. Sexy-sperm hypotheses
   • Good-genes: post-copulatory competition ensures only the highest-quality sperm fertilise eggs.
   • Sexy-sperm: any trait giving sperm a fertilisation edge is heritable; sons inherit superior sperm → indirect fitness.
   • Cricket case study:
     • Sons of polyandrous mothers showed higher sperm viability but no elevated immune function.
     • Supports sexy-sperm, not good-genes, explanation for female multiple mating.

Key Experimental/Statistical References

• Heat-map correlating ornament area & number with fitness (pipefish).
• Cricket sperm-viability ANOVA: differences significant at p<0.05.
• Rodent comparative regression: sperm length correlated with polyandry level (R², slope not quoted in lecture but concept emphasised).

Ethical, Philosophical & Practical Notes

• Bias in historical research reflects human cultural norms (Victorian misogyny); modern science correcting via inclusion of female traits.
• Practical: understanding post-copulatory processes informs pest control, animal breeding, and conservation genetics.
• Philosophical: challenges simplistic narratives of “male competition/female passivity”; reveals fluidity of sex roles across taxa.

Revision Prompts

• Explain how anisogamy underpins classical sexual-selection expectations.
• Using the continuum, place mate plugging and large testes strategies appropriately and justify.
• Contrast good-genes and sexy-sperm hypotheses with an empirical example.
• Describe how CHC scent experiments demonstrated males’ ability to count rivals.

Suggested Reading & Resources

• Parker, G. A. (1970s) seminal papers on dung flies and sperm competition.
• Simmons, L. W. “Sperm Competition and Its Evolutionary Consequences in the Insects” (monograph).
• Moodle quizzes: Lecture 1 revision; Lecture 2 (today) optional self-test.

Looking Ahead

• Next week: mating-systems diversity (monogamy, polygyny, polyandry, polygynandry) & sexual conflict.
• Afternoon lab: continue with individual research projects; opportunities for hands-on sperm-viability staining in microscope lab.