Polygyny carries costs in both sexes in Trinidadian guppies

This study on Trinidadian guppies demonstrates that while increased polygyny boosts male reproductive output, it also imposes significant costs on both sexes, including delayed reproduction and higher failure rates, suggesting that male mating performance is limited and sexual selection pressures may be more balanced between sexes than traditionally assumed.

The Gist

Imagine a bustling fish market where the main attraction is the Trinidadian guppy, a tiny, colorful fish famous for its love life. In the wild, male guppies are often seen as the "players" of the animal kingdom: they are expected to mate with as many females as possible, while females are the ones who get "stuck" with the costs of pregnancy.

The old rule of thumb was simple: "More partners = More babies = Better for the guy."

But a new study by van der Walle and her team suggests this rule might be broken. They ran a laboratory experiment that feels a bit like a dating speed-dating event, but with a twist: they forced the males to choose between two schedules.

The Experiment: The "4-Date" vs. The "7-Date" Week

The researchers set up two groups of male guppies:

1. The "Low Polygyny" Group: Each male was paired with 4 females per week.
2. The "High Polygyny" Group: Each male was paired with 7 females per week.

Think of it like a waiter.

• Waiter A has 4 tables to serve.
• Waiter B has 7 tables to serve.

You might think Waiter B is the superstar, serving more customers and making more money. But the study found that Waiter B was actually burning out.

What Happened to the Females? (The Customers)

When the males were trying to juggle 7 females instead of 4, the females suffered.

• The Delay: Females in the "7-female" group took 9% longer to get pregnant. It's like waiting in a longer line at the grocery store; the cashier (the male) was too busy to ring you up quickly.
• The Failure Rate: The risk of a female never getting pregnant with her assigned male tripled. It's as if the waiter was so overwhelmed he forgot to take the order entirely.
• The Silver Lining: The few females who did get pregnant had slightly larger litters, but only because they were older and bigger, not because the male was a better lover.

What Happened to the Males? (The Waiters)

Here is where the story gets interesting. The "High Polygyny" males (the ones with 7 dates) did eventually win the race, but only if they had a lot of time.

• The Short Term: In the beginning, the "7-date" males were actually slower at getting their females pregnant. They needed 19% more time to get the job done. They were spreading themselves too thin, like a waiter trying to carry too many plates at once and dropping a few.
• The Long Term: It took two months before the "7-date" males finally caught up and surpassed the "4-date" males in total babies produced.
• The Catch: In the wild, guppies live in dangerous rivers full of predators. If a male waits two months to get his reproductive strategy working, he might get eaten before he ever sees the payoff.

The Big Takeaway: "The More, The Better" is a Myth

This study flips the script on sexual selection.

1. Males have limits: Just like a human can't run a marathon at a sprint pace forever, a male guppy has a limit to how many females he can successfully fertilize at once. His "sperm bank" or his "mating energy" gets depleted.
2. It's a two-way street: Usually, we think only females pay the price for bad mating strategies. But here, the males paid a price too: they were slower, less efficient, and risked dying before they could reproduce.
3. Quality over Quantity: In environments where life is short and dangerous (like a river with lots of hungry birds), it might actually be smarter for a male to focus on fewer females to ensure he gets them pregnant fast, rather than chasing a huge harem and failing to deliver.

The Analogy: The Pizza Delivery Guy

Imagine a pizza delivery guy.

• Scenario A: He delivers to 4 houses. He gets there fast, the pizzas are hot, and everyone is happy.
• Scenario B: He tries to deliver to 7 houses at once. He gets lost, the pizzas arrive cold, and some customers cancel their orders.

If the delivery guy is paid by the total number of pizzas sold over a whole year, Scenario B might win eventually. But if he is paid by the speed of delivery, or if he might get mugged on the way (high predation), Scenario A is the winner.

Conclusion

The paper tells us that nature isn't just about "more is better." Sometimes, doing a few things well is better than doing many things poorly. For guppies, being a "player" with a huge harem isn't always the winning strategy; sometimes, being a focused partner is the key to survival.

Technical Summary

1. Problem Statement and Hypothesis

Theoretical Context: Sexual selection theory traditionally posits that males (the sex with lower parental investment) benefit linearly from mating with multiple partners, while females face diminishing returns or costs. This is often visualized as a steeper "Bateman gradient" for males. While costs of polyandry (female multiple mating) are well-documented, the assumption that polygyny (male multiple mating) is universally beneficial for males remains largely untested, particularly in species lacking parental care.

Research Gap: The authors hypothesize that polygyny may impose direct physiological or behavioral costs on males even in the absence of male-male competition or paternal care. Specifically, they investigate whether sperm depletion, ejaculate limitation, or mating fatigue could reduce a male's ability to fertilize females efficiently when spread across too many partners, thereby creating a "cost of polygyny" that negatively impacts both male and female reproductive success.

Study System: The study utilizes the Trinidadian guppy (Poecilia reticulata), a promiscuous, live-bearing fish with no parental care, making it an ideal model to isolate the effects of mating frequency from other confounding factors.

2. Methodology

Experimental Design:

• Subjects: First-generation (F1) laboratory offspring of 297 founders collected from a high-predation stream (Guanapo River) in Trinidad.
• Sample Size: 32 males and 170 females (initially).
• Treatments: Males were assigned to one of two polygyny levels:
  • Low Polygyny: 1 male paired with 4 females ($n=18$ groups).
  • High Polygyny: 1 male paired with 7 females ($n=14$ groups).
• Protocol:
  • Sequential Monogamy: Females were housed individually. Males were moved between female tanks on a weekly schedule.
  • Frequency: Each female was mated once a week. Males had recovery periods in their own tanks.
  • Duration: Mating trials continued until females gave birth or reached 100 days of age.
  • Controls: To ensure male quality was not a confounding variable, males in high-polygyny groups were not necessarily "higher quality" than those in low-polygyny groups; the polygyny level was experimentally imposed.
• Data Collection:
  • Female Metrics: Age at first parturition, first litter size, daily reproductive output (litter size / time to birth), and incidence of reproductive failure.
  • Male Metrics: Number of females fathering offspring, total daily reproductive output, time (mating opportunities) required to initiate pregnancy, and cumulative offspring over time.
• Statistical Analysis: Generalized Linear Mixed Models (GLMMs) were used to analyze reproductive traits. Fixed effects included polygyny level, female age at first mating, pairing order, male death, and recirculation system. Random effects accounted for male identity and maternal lineage.

3. Key Results

Effects on Female Reproduction:

• Delayed Reproduction: High-polygyny females experienced a 9% longer interval between their first mating opportunity and first birth (42.9 days vs. 39.4 days in low-polygyny).
• Reproductive Failure: The risk of reproductive failure (females that did not conceive) was tripled in the high-polygyny group (17.7%) compared to the low-polygyny group (5.6%).
• Litter Size vs. Rate: While high-polygyny females produced larger first litters (30.8% more offspring), this was attributed to them being older at first birth. Their daily reproductive output (offspring per day) was statistically identical to low-polygyny females.
• Fertility Check: Non-reproductive females were not infertile; 95.2% successfully gave birth when paired with new males, confirming the failure was due to the initial male's inability to fertilize.

Effects on Male Reproduction:

• Short-term Costs: High-polygyny males required 19% more mating opportunities (and thus time) to successfully initiate pregnancy in a female compared to low-polygyny males.
• Delayed Benefits: Although high-polygyny males eventually fathered offspring with 49% more females and achieved a 73% higher total daily reproductive output, these benefits were delayed. High-polygyny males only surpassed low-polygyny males in cumulative offspring count after 65 days.
• Failure Rates: High-polygyny males had a significantly higher fraction of non-reproductive females in their harem.

4. Key Contributions

1. Quantification of Male Costs: The study provides empirical evidence that polygyny is not cost-free for males, even in species without parental care. It challenges the "more is better" assumption by demonstrating that spreading mating effort too thinly reduces fertilization efficiency.
2. Bidirectional Costs: It demonstrates that male mating performance limits directly translate into reproductive costs for females (delayed conception, higher failure rates), creating a feedback loop where male polygyny reduces overall group reproductive output.
3. Mechanism of Limitation: While the exact mechanism (sperm depletion vs. mating fatigue) was not pinpointed, the results strongly suggest that male ejaculate or mating performance is a limited resource that saturates at high female densities.
4. Ecological Implications: The findings suggest that in high-predation environments (where guppies face high extrinsic mortality), the optimal polygyny level for males might be lower than previously thought. If a male cannot fertilize a female quickly, both may die before reproduction occurs, selecting against extreme polygyny.

5. Significance

• Paradigm Shift: The study contributes to a growing paradigm shift in sexual selection theory, suggesting that sexual selection operates on females as well as males. If polygyny carries costs for males, it implies the existence of male mate choice or constraints on male mating performance.
• Evolutionary Dynamics: It suggests that the strength of sexual selection may be more similar between sexes than traditionally assumed, particularly in environments with high extrinsic mortality where rapid reproduction is critical.
• Conservative Estimates: The authors note that their experimental design (eliminating male-male competition and restricting to first litters) likely underestimates the true costs of polygyny in the wild, where competition and multiple litters would further penalize inefficient males.

In conclusion, van der Walle et al. demonstrate that in Trinidadian guppies, increased polygyny imposes significant reproductive delays and failure risks on females and reduces the immediate reproductive efficiency of males, challenging the notion that male reproductive success scales linearly with mate number.