Persistent male survival advantage in a protogynous hermaphrodite fish

Contrary to the typical expectation of higher male mortality in polygynous species, a study on the protogynous cleaner wrasse *Labroides dimidiatus* during the 2024 El Niño event revealed that terminal-phase males exhibited greater survival than initial-phase females, whose mortality more than doubled due to physiological vulnerabilities linked to faster growth rates.

The Gist

Imagine a bustling underwater city called the Great Barrier Reef. In this city, there's a special kind of fish called the Cleaner Wrasse. Think of them as the reef's "barbers" or "doctors." They swim around other fish, eating parasites off their skin, which keeps the whole ecosystem healthy.

Here's the twist: These fish are shape-shifters. They start their lives as females. But as they grow bigger and stronger, a few of them decide to change into males. Once they become males, they become the "bosses" of small groups (harems) of females.

The Big Question: Who Survives the Storm?

Scientists usually have a rule of thumb for animals: Males often die younger. Why? Because being a male is expensive. They fight each other, they need to be huge to win, and they burn a lot of energy. When the weather gets bad (like a heatwave), scientists expect the males to be the first to crash and burn.

But the researchers in this study wanted to see if this rule holds true for these shape-shifting fish, especially during a massive heatwave called El Niño that hit the reef in 2024.

The Experiment: A Two-Year Watch

The scientists acted like underwater detectives. They spent two years diving around Lizard Island, tracking 731 individual fish. They gave them little tattoos (using safe, colorful dyes) or recognized them by their unique "fashion" (color patterns).

They watched these fish through:

1. Normal times: When the water was cool and the coral was happy.
2. The "Heatwave" (2024 El Niño): When the water got 1 degree hotter than usual, causing massive coral bleaching (like a sunburn for the reef) and killing off food sources.

The Shocking Discovery: The Bosses Won the Race

The results flipped the script completely.

• The Expectation: The "male bosses" should have struggled the most because they are big and need lots of food.
• The Reality: The females died at more than double the rate of the males during the heatwave.

It was as if the "employees" (females) were getting sick and leaving the city, while the "bosses" (males) stayed strong and healthy.

Why Did This Happen? (The Analogy)

The researchers came up with a few clever theories to explain this:

1. The "Growth vs. Survival" Trade-off:
   Imagine the females are like sprinters. They grow very fast, trying to get big enough to eventually become males. This fast growth burns a lot of energy. When the "food truck" (the reef) stops coming because of the heatwave, the sprinters run out of gas first. The males, who have already finished growing and are just "maintaining" their size, are more like marathon runners. They are efficient and can survive on less energy.

2. The "Survivor" Effect:
   To become a male, a fish has to survive the tough female phase first. It's like a survival of the fittest filter. Only the strongest, healthiest females make it to the "male" stage. So, the males are essentially a "super-selected" group of the toughest fish in the population. When the heatwave hit, these tough guys had the best chance of making it through.

3. The "Egg" Burden:
   Females are constantly trying to make eggs, which takes a huge amount of energy. During the heatwave, when food was scarce, trying to make eggs while also growing fast was a recipe for disaster. The males didn't have this extra burden.

What Does This Mean for the Future?

This study is a wake-up call for how we understand climate change.

• Old Thinking: We assumed that in many animal groups, the males are the weak link when things get tough.
• New Thinking: In species that change sex, the "male" phase might actually be the resilient phase.

This is good news for the reef's future. Because these fish can change sex, if the population gets knocked down, the surviving males can wait, and new females can grow up and eventually turn into males to take over. The system is flexible.

In short: When the ocean gets hot, the "bosses" of the cleaner fish world turned out to be the toughest survivors, while the "workers" (females) struggled the most. Nature is full of surprises, and sometimes the rules we think we know need a complete rewrite!

Technical Summary

1. Problem Statement

In polygynous species with fixed sexes (dioecious), males typically face higher mortality than females due to intense intrasexual competition, larger body sizes, and higher energetic demands. This "male-biased mortality" is expected to intensify under climate change and environmental stress (e.g., heatwaves). However, it remains unclear how these dynamics apply to protogynous hermaphrodites (species where individuals start as females and change sex to males later in life). Specifically, the study addresses a critical gap: how sex change and sex-specific life-history strategies influence survival and growth resilience during extreme climatic events, such as El Niño–Southern Oscillation (ENSO) events, which cause marine heatwaves and coral bleaching.

2. Methodology

• Study Species & Site: The study focused on the cleaner wrasse (Labroides dimidiatus), a keystone protogynous species on the Great Barrier Reef. Research was conducted at eight reef sites around Lizard Island, Australia.
• Study Period: Data were collected over two years (2023–2024), encompassing the 2024 ENSO event, which caused a 1°C temperature increase, severe coral bleaching, and mortality at the study site.
• Data Collection:
  • Census: 731 adult fish and 495 juveniles were tracked. Adults were individually identified using Visual Implant Elastomer (VIE) tags (up to 1,296 unique codes) or distinct natural color patterns.
  • Sex Identification: Sex was determined via behavioral observations (e.g., "Flutter-Run" displays by males, "Body-Sigmoid" by females, spawning roles) and confirmed by spawning patterns (males spawn with smaller partners; females with larger ones). 42 individuals were observed changing sex during the study.
  • Growth Measurement: A calibrated underwater stereo-photogrammetric system (two GoPro cameras) was used to measure fish length with high precision (error ±1.13–1.81 mm).
  • Environmental Context: Water temperature data from AIMS buoys and in-situ coral bleaching surveys (photo-quadrats) were used to confirm the severity of the 2024 thermal stress.
• Statistical Analysis:
  • Density: Generalized Linear Mixed Effects Models (GLMM) with log-transformed density data.
  • Growth: Linear Mixed Effects Models (LMER) and GLMMs with Tweedie distributions to analyze growth rates across size classes, seasons, years, and sexes.
  • Survival: LMER with arcsine square root transformation to analyze mortality rates, including fixed effects for sex, period, and their interaction, with site as a random effect.

3. Key Results

• Environmental Impact: The 2024 ENSO event resulted in Degree Heating Weeks (DHW) >8, causing widespread coral bleaching and a 17.44% decline in overall cleaner wrasse density compared to 2023.
• Survival Disparity (The Core Finding): Contrary to the expectation of male-biased mortality in polygynous systems, males exhibited significantly higher survival rates than females.
  • Baseline (2023): Female mortality was estimated to be 7–8 times higher than male mortality.
  • ENSO Event (Summer 2024): Female mortality more than doubled compared to the previous summer, while male mortality remained stable and unaffected by the thermal stress.
  • Interaction: The sex difference in mortality was statistically significant in Summer 2023, Winter 2023, and Summer 2024, but not in Winter 2024.
• Growth Dynamics:
  • General Trend: Growth rates declined significantly for both sexes during the 2024 ENSO summer compared to other periods.
  • Sex Differences: Under normal conditions (2023), females grew significantly faster than males (approx. 44–100% faster depending on season). However, during the 2024 ENSO, this sex-based growth difference disappeared, as environmental stress suppressed growth in both sexes equally.
  • Size Classes: Reduced growth in 2024 was most pronounced in 50 mm and 70 mm size classes.

4. Key Contributions

• Challenging Established Theory: The study overturns the general assumption that males in polygynous systems are more vulnerable to mortality. It demonstrates that in protogynous hermaphrodites, the terminal sex (males) can possess a persistent survival advantage.
• Mechanism of Resilience: The authors propose that male survival advantage may stem from:
  1. Selective Filtering: Males are a "survivor cohort" that has already successfully navigated the female phase and the associated energetic costs of growth and egg production.
  2. Energetic Trade-offs: Females face a dual energetic burden (current reproduction + growth for future sex change), making them more vulnerable to resource limitation and thermal stress.
• Climate Change Demography: The research highlights that climate extremes do not affect sexes equally, even within hermaphroditic species. Females act as the "canary in the coal mine," suffering disproportionate mortality during thermal stress.

5. Significance

• Population Dynamics: The findings suggest that protogynous populations may be more resilient to climate extremes than previously thought because the reproductive males (the limiting factor for harem maintenance) are highly resilient. Furthermore, because sex change is socially controlled and new reproductive individuals are always females, sex ratios can rapidly re-equilibrate after female mortality events.
• Conservation Implications: While protogynous species are often vulnerable to overfishing (which targets large males), this study suggests that climate-driven mortality may disproportionately impact females. This shifts the focus of conservation strategies for these species, emphasizing the need to protect female cohorts and their habitats during extreme weather events.
• Broader Ecological Context: As cleaner wrasses are keystone species affecting reef health and diversity, their specific demographic responses to climate change have cascading effects on the broader reef ecosystem. The study underscores the necessity of incorporating sex-change mechanisms into models predicting species' responses to global warming.