Marine Science: Analyzing Sex

The Challenge

Anthropogenically induced climate change is one of the most serious and pervasive global challenges (Hoegh-Guldberg & Bruno, 2010; Diffenbaugh & Field, 2013). To minimize adverse outcomes, it is critical to establish and enforce effective ecosystem management (Hoegh-Guldberg & Bruno, 2010), which in turn depends on a robust understanding of organism and ecosystem resilience to environmental change (O’Leary et al., 2017; Patricio et al., 2019). We do not yet sufficiently understand the extent to which such resilience varies with sex.

The sex ratio of a population is a main determinant of its resilience to environmental disturbance (Ospina-Alvarez & Piferrer, 2008). Sex ratios are driven in part by differential sensitivity of females, males and hermaphrodites to climate change stressors. Nonetheless, sex is rarely analyzed as an experimental variable (Tannenbaum et al., 2019). A recent systematic review of ocean acidification literature, for example, revealed that only 3.77% of recent studies tested for sex-based differences (see figure below), while 85% of studies failed to consider sex at all (Ellis et al., 2017). This results in a lack of experimental evidence on which to assess sex-specific impacts of ocean acidification, limiting our ability to accurately appraise the resilience of marine populations to reduced seawater pH. Where tested, clear sex-based differences to elevated pCO2 have been documented (Ellis et al., 2017). Failing to account for such differences impacts our ability to effectively manage ecosystems and to determine conservation priorities.

Gendered Innovation 1: Understanding Feminization in a Warming Ocean

Temperature-dependent sex determination (TSD) in marine turtles is perhaps the most widely studied and well-known mechanism of environmental sex determination in nature. However, species that exhibit TSD are also widely considered among the most vulnerable to climate change given the possibility that increasing temperatures favor the production of one sex over the other, destabilizing population sex ratios (Mitchell & Janzen, 2010). In marine turtles, sex is determined by temperature during egg incubation, with higher temperatures resulting in a greater proportion of females (Hawkes et al., 2007; Hawkes et al., 2009; Patricio et al., 2019).

Studies have projected highly female-skewed population sex ratios in marine turtles based on future climate warming, using temperature recordings during incubation as a proxy for population demography (e.g. Hawkes et al., 2007; Fuentes et al., 2011; Laloë et al., 2014). Such sex ratio estimates, however, depend on the proxy used in sex determination, and may differ substantially when different proxies are used (Fuentes et al., 2011).

Recent advances in the sexing of marine turtles, which combine laparoscopic and endocrinological techniques, have, for the first time, provided empirical evidence for the impact of recent warming on contemporary marine turtle populations. Robust sex analysis enabled the researchers to link male and female green sea turtles to their natal beaches, leading to the discovery that northern (warmer) Great Barrier Reef populations have become highly female biased. Over 99% of juveniles and sub-adults originating from northern sites are female (compared to 67% female at southern sites) (Jensen et al., 2018). Despite the ability of marine turtles to maintain population viability even at highly female-biased sex ratios, a subadult female bias of 99.8% in northern green sea turtle populations indicates that the complete feminization, and thus local extinction, of northern GBR populations is possible in the near future (Jensen et al., 2018).

Gendered Innovation 2: Understanding Environmental Sex Determination beyond Temperature

Sex determination mechanisms fall on a continuum from environmental (ESD) to genetic (GSD). Primary sex differentiation has been shown to respond to a diverse range of environmental factors in a growing number of species. Hypoxia, for example, results in a higher ratio of males in zebrafish (Shang et al., 2006). Ocean acidification, in contrast, results in 16% more female oysters over a single generational cycle (Parker et al., 2018). Similarly, increased aquatic pH results in more female cichlids (Oldfield, 2005). What is increasingly apparent is that alterations in sex ratio—in either direction—will result in populations less resilient to further disturbance and potentially lead to demographic collapse. A mechanistic understanding of sex-change processes and other ecologically significant sex-based responses is thus vital to accurately modelling impacts of anthropogenic disturbance (e.g. overfishing or climate change) at a population level.

Gendered Innovation 3: Sex Analysis Enhances Effective Population Management

An accurate understanding of population structures enhances effective ecosystem management. Recent advances in next-generation sequencing technology has facilitated research focused on the causes and consequences of changes in population structure in a wide range of non-model species (Narum et al., 2013). However, only 9.6% of studies on marine and diadromous (tolerant of both seawater and freshwater) species have reported sex information (Benestan et al., 2017).

Benestan and colleagues (2017) demonstrate the importance of understanding sex ratios when employing sequencing to interpret population structure. In the American lobster, for example, these authors demonstrate how two populations (inshore and offshore) can be misunderstood as two distinct subpopulations if the sex ratio of samples is unintentionally biased. Studies that sample correctly, i.e. take care to collect equal numbers of males and females, show that in reality inshore and offshore American lobsters are a connected population that is mixed genetically. Omitting sex information in this instance leads to the incorrect classification of two distinct populations, which in turn may result in ineffective management recommendations.

The American lobster is the most valuable catch in North America. Effective population management has been demonstrated to successfully maximize its sustainable exploitation. Proactive harvester-driven conservation of commercial stocks in the Gulf of Maine, for example, has resulted in record hauls, despite warming (Le Bris et al., 2018). Conversely, in the absence of such management, warming has led to the collapse of the fishery in southern New England (Le Bris et al., 2018).

Accurate population demographic data is especially important when conservation efforts are sex biased. Lobster conservation efforts have protected large berried females (females carrying fertilized eggs on the underside of the abdomen), but not large males. This female-biased protection leads to selective harvesting of large males, which subsequently restricts mate choice and limits sperm, resulting in reduced reproductive success (Tang et al., 2019). In the face of climate change, effective management of this natural resource will become increasingly critical to preserve the reproductive potential of lobster stocks. Robust sex analysis will ensure population structure is understood, and thus managed and protected accurately.

Gendered Innovation 4: Understanding the Differential Sensitivity of Female and Male Marine Organisms to Climate Change

Anthropogenically induced climate change results in rising seawater temperatures, ocean acidification, hypoxic zones and storm events. Where tested, sex analysis has emerged as a key parameter for determining species responses to these environmental challenges. Elevated seawater pCO2 (dissolved carbon dioxide), for example, results in differential mortality between the sexes in Crustacea. Both female shrimp (Kurihara et al., 2008) and copepods (Cripps et al., 2014) show greater sensitivity to climate change than their male counterparts.

This pattern, however, does not always hold and analyses must be done carefully. In the copepod Arcatia tonsa, females show greater tolerance of elevated temperatures (Sasaki et al., 2019). Failing to account for sex differences in response to elevated temperatures risks underestimating population-level impacts by overlooking population decline caused by sperm limitation from greater male temperature sensitivity.

Sex differences in response to climate change can be complex. A recent study of copepod response to elevated pCO2 by Cripps and colleagues (2016) demonstrated this complexity. Under normal conditions, males have a higher baseline metabolic rate than females. In response to elevated pCO2, however, females increase and males decrease their metabolic rate (Cripps et al., 2016). Omitting sex analysis in this case masks sex-specific responses in physiological performance that are fundamental for determining population responses.

The differential sensitivity of female and male organisms to changing environmental conditions can also have a large, indirect and often unexpected impact on experimental outcomes. In marine copepods, for example, environmental conditions influence where individuals aggregate in the water column. Studies have shown that differential energy and reproductive requirements lead females to aggregate primarily in oxygenated surface layers of the water; males cluster in deeper water where oxygen concentrations are lower, as their location is primarily driven by temperature (Pierson et al., 2017). If this behavior is overlooked, researchers collecting specimens from a single depth would inadvertently introduce a sex ratio bias that would yield incorrect experimental conclusions.