Behavioral Ecology P4

Foundations of Mating Systems and Anisogamy

• Variability in Parental Investment and Mating Systems

  • In species such as bowerbirds, males invest minimal energy in offspring beyond their sperm. Their entire reproductive effort is concentrated on courting females. Because female bowerbirds are selective, mating success among males is highly skewed.
  • In a study of $34$ male bowerbirds, the $6$ most successful males accounted for $53\%$ of all matings (Uy et al., 2001).      
  • Bowerbirds are categorized as polygynous, a mating system where each successful male mates with multiple females while females raise the young alone.
  • Conversely, species like the blue tit (Parus caeruleus) exhibit pair bonding where both parents collaborate to incubate eggs and feed offspring.      
  • Blue tits are classified as socially monogamous, meaning males and females form long-term pairs, but they are not strictly monogamous. Females frequently engage in extra-pair copulations with neighboring males. Consequently, highly attractive male blue tits achieve higher reproductive output than less attractive males, though the variance in male success is not as extreme as in polygynous species like bowerbirds.

• Anisogamy as the Fundamental Evolutionary Driver

  • Biological differences in mating behavior, female selectivity, and parental investment stem from anisogamy—the asymmetry in gamete size and production costs between sexes.      
  • Male Gametes (Sperm): Small, plentiful, highly mobile, and energetically inexpensive to produce.
  • Female Gametes (Eggs): Large, few in number, immobile, and energetically costly to produce.
  • Because female reproductive output is limited by the number of eggs produced rather than the number of mates, females experience selective pressure to be choosy about their mates. Male reproductive output is limited primarily by access to receptive females, driving intense competition among males for mating opportunities.

Sexual Selection Mechanisms

• Overview and Sexual Dimorphism

  • Differential reproductive success caused by competition for mates drives sexual selection, a distinct form of natural selection first described by Charles Darwin.
  • Sexual selection accounts for differences in mating behavior and the prevalence of sexual dimorphism, wherein males and females display contrasting physical phenotypes.

• Intrasexual Selection and Weaponry

  • Intrasexual selection involves direct competition between members of the same sex (typically males) for access to mates.
  • Contests often rely on physical battles or displays of strength, selecting for exaggerated weapons such as horns, antlers, tusks, and claws.
  • Example: Male giant Japanese rhinoceros beetles (Trypoxylus dichotomus) use long head horns—present exclusively in males—to dislodge competitors from tree sap feeding sites where females feed.
  • Example: Species such as elk, sea lions, frogs, and fiddler crabs engage in physical contests using specialized structures.
  • Paradox of Weaponry: Exaggerated weapons can reduce injuries by serving as honest signals of body condition, allowing smaller or weaker individuals to yield without engaging in costly or fatal conflicts.

• Intersexual Selection (Female Choice)

  • Intersexual selection occurs when individuals of one sex (typically females) actively choose among potential mates of the opposite sex.
  • Drives the evolution of elaborate male ornaments, vocalizations, and courtship displays.
  • Example: Long-tailed widowbirds (Euplectes progne) are passerine birds inhabiting African savannas. During the non-breeding season, males possess drab, camouflaged tan plumage. In the breeding season, males molt into jet-black plumage with bright red and yellow wing patches and grow tail feathers measuring approximately $0.5\,\text{m}$ in length, allowing them to be spotted from up to $1\,\text{km}$ away. Polygynous males use aerial displays and territory defense to attract multiple females.

Experimental Evidence for Female Choice: Long-Tailed Widowbirds

• Experimental Setup (Andersson 1982)

  • Swedish evolutionary biologist Malte Andersson tested whether female widowbirds prefer extravagantly ornamented males (H1) or choose mates based on territory quality (H2).
  • Andersson manipulated male tail length across four experimental groups:
  1. Shortened: Tail clipped by approximately $25\,\text{cm}$.
  2. Lengthened: Clipped feathers glued onto existing tail feathers to extend length.
  3. Cut & Reglued (Control 1): Tail cut and immediately glued back on to control for handling and glue effects.
  4. Uncut (Control 2): Captured and released without tail modification.      
  • Mating success was quantified by counting the number of new nests established in each male's territory during the remainder of the breeding season.

• Results and Implications

  • Prior to treatment, mean initial nest numbers did not differ significantly among groups.
  • Following treatment, males with artificially lengthened tails secured a significantly higher mean number of new nests compared to all other groups. Shortened males did not suffer a statistically significant decrease compared to control groups.
  • The findings supported H1, demonstrating direct female preference for male ornamentation.
  • Evolutionary Trade-offs: Unnaturally long tails confer a mating advantage, but natural tail length represents an evolutionary trade-off balancing the reproductive benefits of female attraction with the survival costs of increased predation risk and energy expenditure during flight.

Indirect Benefits and Female Choice Models

• Direct vs. Indirect Benefits

  • Direct Benefits: Immediate material gains provided by males, including territory resources, parental care, nuptial gifts, and physical protection.
  • Indirect Benefits: Genetic advantages passed to offspring when males contribute only sperm.

• Good Genes Hypothesis

  • Elaborate male ornaments function as honest signals of underlying genetic quality, such as disease resistance, high immunocompetence, or overall vigor.
  • Handicap Principle: Extreme traits represent a physical handicap; only superior males possess the energy and vitality to survive despite the handicap.

• Runaway Sexual Selection ("Sexy Sons" Hypothesis)

  • Proposed by Ronald Fisher; female preference for a male trait creates a positive evolutionary feedback loop.
  • Females preferring an exaggerated trait produce sons carrying genes for the trait and daughters carrying genes for the preference.
  • Trait and preference co-evolve to extreme levels until countered by severe natural selection survival costs.

• Case Study: Indian Peafowl (Pavo cristatus)

  • Peacocks aggregate in communal display grounds called leks to court peahens.
  • Research by Marion Petrie, Adeline Loyau, Roslyn Dakin, and colleagues revealed:
  • Male mating success (number of copulations) correlates positively with tail mass and the total number of eyespots (ocelli).
  • Experimental removal of eyespots causes a measurable decline in male mating success.
  • Peacocks with greater eyespot counts possess stronger immune systems and suffer lower mortality from fox predation.
  • Controlled breeding experiments demonstrate that peacocks with larger mean eyespot areas sire offspring with higher survival rates when released into natural environments.
  • Tail morphology features display significant heritability.
  • Empirical evidence supports both the Good Genes hypothesis and Runaway Sexual Selection in shaping peafowl train evolution.

Alternative Male Mating Strategies

• Intrasexual Competition and Small Male Alternatives

  • In species governed by male-male combat, smaller males face low probabilities of winning direct contests. Selection favors alternative tactical strategies that bypass physical combat.

• Case Study: Precocious Parr in Atlantic Salmon (Salmo salar)

  • Atlantic salmon exhibit two distinct male life history phenotypes:
  • Migratory Males: Migrate to sea, feed and grow for up to $3\,\text{years}$, and return as large adult competitors.
  • Precocious Parr: Remain in their natal river, achieving sexual maturity in approximately $1\,\text{year}$ at a much smaller body size.
  • Behavioral Mechanism: Precocious parr hide near spawning pairs and rapidly dart in to release sperm simultaneously as the large migratory male and female spawn.
  • Costs and Benefits: Precocious parr avoid the high mortality associated with ocean migration and combat, increasing their likelihood of surviving to reproduce, but produce smaller absolute volumes of sperm per spawning event.
  • Genetic analyses show that sneaker males sire up to $60\%$ of juvenile fish in certain Atlantic salmon populations.

• Evolutionarily Stable Strategies (ESS)

  • An Evolutionarily Stable Strategy (ESS) is a strategy or combination of strategies that cannot be invaded by an alternative strategy when adopted by a population at equilibrium.
  • The co-existence of migratory males and sneaker parr represents a mixed ESS maintained by negative frequency-dependent selection (each phenotype achieves highest relative fitness when comparatively rare).

Parental Care, Trade-offs, and Paternity Certainty

• Parental Investment Patterns Across Vertebrates

  • Parental investment encompasses allocation of resources toward current offspring at the expense of parental survival or future reproduction.
  • Mammals: Internal gestation and lactation obligate female care, resulting in female-only care in $91\%$ of mammalian species.
  • Birds: Both sexes can incubate eggs and provision chicks, leading to biparental care in $81\%$ of bird species.
  • Fishes, Amphibians, and Reptiles: Most species provide zero post-zygotic care; offspring are precocial and self-sufficient upon hatching.

• Paternity Certainty and Cuckoldry

  • Males gain no evolutionary fitness by expending resources on non-kin. Male parental investment is constrained by certainty of paternity.
  • In species with external fertilization, paternity certainty is generally higher than in internal fertilizers, favoring the evolution of male parental care.

• Case Study: Bluegill Sunfish (Lepomis macrochirus) Experiments (Neff 2003)

  • Male bluegill sunfish display two main life history strategies:
  • Parental Males: Large, territorial males that build nests, attract females, and guard eggs and fry.
  • Cuckolders: Small sneaker males that dart into nests during spawning, and larger female mimics that copy female behavior to participate in three-way spawning events.
  • Parental males assess paternity using two distinct cues:
  1. Visual Cues (Egg Stage): Observing rival sneaker males nearby during spawning reduces paternity confidence.
  2. Olfactory Cues (Fry Stage): Males smell waterborne chemical cues produced by newly hatched fry to determine direct genetic relatedness.      
  • Experiment 1 (Visual Cue Manipulation):
  • Treatment parental males were exposed to sneaker males enclosed in clear plastic cages during spawning.
  • Treatment males significantly reduced care allocated to eggs compared to control males ($t_{39} = 2.7$, $P = 0.011$).
  • Once eggs hatched into fry, treatment males restored care to levels statistically indistinguishable from controls because olfactory cues confirmed genetic paternity.      
  • Experiment 2 (Direct Paternity Manipulation):
  • Parental males spawned in isolation (high initial paternity confidence).
  • Experimenters swapped approximately $\frac{1}{3}$ of the eggs in treatment nests with eggs from other males.
  • The day after egg swapping, treatment and control males provided identical care to eggs (males could not visually distinguish foreign eggs).
  • The day after hatching, treatment males provided significantly less care to fry than control males ($t_{27} = 2.1$, $P = 0.047$) as olfactory cues revealed reduced paternity.

Mating Systems, Fitness Variance, and Sexual Conflict

• Classification of Mating Systems

  • Monogamy: One male mates with one female. Favored when resource scarcity requires biparental care for offspring survival.
  • Polygyny: One male mates with multiple females. Favored when resources or females are clumped and defendable.
  • Polyandry: One female mates with multiple males. Rare; associated with male-only parental care and reversed sexual dimorphism (e.g., Red-necked Phalaropes, where females are larger and more brightly colored).
  • Polygynandry: Multiple males mate with multiple females.

• Fitness Variance and Sexual Dimorphism

  • Mean fitness is statistically identical between males and females in sexually reproducing populations with an even sex ratio.
  • Variance in Fitness differs dramatically depending on the mating system:      
  • Polygynous (Indian Peafowl): High male fitness variance (few males obtain many matings, many males obtain zero) and low female fitness variance. Strong sexual dimorphism.
  • Monogamous (Herring Gull): Low and equal fitness variance between sexes. High degree of sexual monorphism.
  • Polyandrous (Red-necked Phalarope): High female fitness variance and low male fitness variance. Reverse sexual dimorphism.

• Sexual Conflict and Extra-Pair Copulations

  • Sexual Conflict arises when evolutionary strategies to maximize individual fitness differ between males and females.
  • In socially monogamous species like blue tits, both sexes seek extra-pair copulations whenever the behavior yields net fitness gains.
  • Male stag beetles (Lucanidae) utilize exaggerated mandibles in combat to control feeding sites visited by females, illustrating resource-defense polygyny.

Review Questions and Analytical Case Studies

• Question Check Details & Analytical Summaries
  • Sexual Selection Dynamics: Male-male competition generates enhanced male weaponry (e.g., horns, antlers), whereas female choice drives male ornamentation (e.g., gaudy tail plumage).
  • Paternal Care Likelihood: Paternal care is most likely in monogamous species with high paternity certainty (e.g., great spotted woodpeckers).
  • Southern Elephant Seal Case Study: Highly polygynous "beachmasters" defend large harems on beaches. Non-pregnant females avoid harem stress by staying at sea, mating with subordinate males. Small males maximize fitness by seeking matings at sea when beach harems are monopolized by dominant males.
  • Sandfly (Lutzomyia longipalpis) Mate Choice Case Study:      
  • Experimental data demonstrate that female sandflies mating with attractive males obtain no direct benefits (no increase in egg output or female longevity). However, fathers with high attractiveness sire sons with significantly higher mating success. This confirms that female sandflies choose mates based on indirect benefits in the form of attractive male offspring ("sexy sons").