Using YY supermales to destabilize invasive fish populations

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Abstract

A plausible biocontrol strategy for the eradication of invasive species involves augmenting wild populations with genetically modified supermales. Supermales contain double YY chromosomes. When they are augmented into a wild population, destabilization and eventual extinction occurs over time due to a strongly skewed gender ratio towards males. Here, we employ a mathematical model that considers an Allee effect, but we have discovered through simulation that the presence of supermales leads to an increase in the minimal number of females needed for survival at a value higher than the mathematically defined Allee effect. Using this effect, we focus our research on exploring the sensitivity of the optimized supply rate of supermale fish to the initial gender ratio and density of the wild populations. We find that the eradication strategy with optimized supply rate of supermales can be determined with knowledge of reproductive rate and survival fitness of supermale fish.

Introduction

Invasive aquatic species continue to be an escalating problem throughout the world. Upon successfully establishing themselves in a new environment, they can be difficult to manage and virtually impossible to eradicate and the control costs can become prohibitive. In an effort to find a better method for eradicating invasive fish species, a sex-skewing technique originally described by Scott et al. (1989), might be used as an autocidal biocontrol strategy in the invasive fish population. Gutierrez and Teem (2006) proposed an autocidal biocontrol TrojanY-Chromosome (TYC) strategy to eliminate invasive alien species with an XXXY sex-determination system via a constant release of sex-reversed supermales. Many fish species with an XXXY sex-determination system have separate sexes throughout life, a condition known as gonochorism. However, some fish species exhibit sequential hermaphroditism (viz., parrotfish, damselfish) or simultaneous hermaphroditism (viz., Serranidae) (Devlin and Nagahama, 2002). Therefore, the TYC eradication strategy is particularly relevant to gonochoristic fish species (which do not exhibit sequential or simultaneous hermaphroditism) with an environmentally reversible XXXY genetic sex determination system. Other life-history characteristics important for sex-reversal in captive breeding includes fishes with sexual dimorphism and rapid life-cycles that would allow subsequent generations of fish to spread rapidly.

Exogenous sex hormones are used widely to manipulate gender in aquaculture fishes. Exposure to certain sex hormones can feminize XY fish (Scott et al., 1989). Since feminization of XY male fish using sex reversal hormones (viz. estrogen) sometimes becomes inefficient due to the stronger tolerance of some fish species to estrogens (Shelton, 1986, Teem and Gutierrez, 2010), another viable way to produce fertile female XY fish is by treating XY male fish using estrogen together with exogenous Flutamide to block the function of endogenous androgen (Jiang et al., 2018). The XY phenotypic female (neofemale) fish when mated with wild type XY male fish produce 25% wild-type XX females, 50% wild-type XY males and 25% YY supermales. YY supermale fish can also be produced by using androgenesis which does not involve in feminization (Jiang et al., 2018). Crossing these homozygous YY supermales with wild-type females yield 100% male offspring (cf. Fig. 1). The TYC strategy has been used to obtain YY supermales in a variety of fish, including Nile tilapia (Mair et al., 1997, Vera Cruz et al., 1999), yellow catfish (Liu et al., 2013), and brook trout (Schill et al., 2016). Further, Gutierrez and Teem (2006) proposed to supply feminized YY supermales into an undesired population that would produce YY supermales and XY males only. Since YY supermales are more resistant to feminization than wild type XY species (Liu et al., 2013, Mair et al., 1997), by considering the cost-effectiveness of the eradication strategy, a constant rate of injection of non-feminized supermales to the target invasive fish population seems more viable. Under the assumption that our target fish species have an XXXY system of sex determination and supermale fish can survive and reproduce successfully, a constant supply of non-feminized supermale fish into the system would generate 75% of wild-type male progeny and 25% wild-type female progeny, skewing the sex ratio towards the dominance of males (cf. Fig. 1) (Wang et al., 2016).

At low population density, the per-capita growth rate can be related positively to the population density, a phenomenon broadly referred to as an Allee effect (Courchamp et al., 1999, Stephens and Sutherland, 1999). In the context of marine fishes, researchers observe that an Allee effect is significant at very low population size and with bias in sex ratio (Perälä and Kuparinen, 2017, Wedekind, 2012). There is strong statistical evidence that the local extinction of Atlantic cod (Gadus morhua) in the southern Gulf of St. Lawrence and the collapse of Atlantic herring (Clupea harengus) population in the North Sea are due to predation-driven Allee effect (Neuenhoff et al., 2018, Perälä and Kuparinen, 2017). A population with the sex ratio biased towards males would lead to difficulty in finding a mate, even if it utilizes powerful sex pheromones. Such biased sex ratios strengthen pre-existing Allee effects due to mating failure, thereby increasing the risk of population extinction. The model developed here considers a constant supply of non-feminized supermale invasive fish as a biocontrol of the invasive fish species. By considering Allee effects in an invasive fish population and a continual injection of non-feminized supermale invasive fish above some critical threshold, the rarity of wild-type females would lead to difficulty in finding mates, and so the invasive fish population would be likely to eventually become locally extinct. However, it is not economically viable to keep introducing supermales indefinitely. The time for terminating the supply of supermales is critical to preventing the wild-type invasive species from recovering in the absence of supermale invasive fish (Wang et al., 2014).

In this paper, our goal is to find the minimum viable supply rate of supermale invasive species together with the minimum window of time required to inject the supermales and successfully get rid of the wild-type invasive fish population. We also determine how the minimum time for supplying the supermales varies with the supply rates above its minimum threshold for eliminating the wild-type population. Researchers (Bayraktarov et al., 2014) observed that there can be a significant variation in the population density of the invasive fish across its non-native ranges. Therefore, we need to analyze how the optimized management strategy might change as a function of initial gender ratio and population density of the wild-type invasive fish population. Since the YY supermales might not be as reproductively fit as that of the wild-type fishes (Kennedy et al., 2018, Schill et al., 2017), we analyze how the minimum viable supply rate and the minimum continual supply time varies with the reproductive fitness and survival fitness of supermale species.

Section snippets

Model equations

For the model described below, FXX(T), MXY(T) and SYY(T) represent the population density of wild-type female invasive fish, wild-type male invasive fish and non-feminized supermale invasive fish, respectively, at time T. The rate of injection of supermale invasive fish is μ0 (time−1 density−1). The reproduction rate of wild-type invasive fish species due to the interactions between male and female wild-type invasive fish species is β1 (time−1 density−2), whereas the reproduction rate of

Results

Discussion

This study is intended to present a theoretical analysis of a biocontrol strategy to eliminate invasive fish from marine protected areas by considering a mathematical model of three genotype/phenotype variants of the invasive fish species with Allee effect. The proposed model is essentially a modified version of the classical TYC model (Gutierrez and Teem, 2006) which satisfies the non-negativity conditions and prevents blow-up of solutions in a finite time (Parshad et al., 2019). The model

Acknowledgments

JB is supported by the grants from Science and Engineering Research Board (SERB), Govt. of India (File No. TAR/2018/000283). SB acknowledges financial support in the form of J C Bose Fellowship by the SERB, Govt. of India , no. SB/S2/JCB-023/2015.

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