The population-level impacts of endocrine disrupting chemicals in fish
Coe, Tobias Sayer
Thesis or dissertation
University of Exeter
Endocrine disrupting chemicals (EDCs) are one of the many anthropogenic pollutants released into the environment. There is a substantial body of literature that has shown a detrimental impact on wildlife, particularly aquatic species, following exposure to these pollutants. In particular, exposure to EDCs can cause disruptions in sexual development and reproductive function. The majority of the effects observed are alterations in the physiology and behaviour of individuals and a key research question that has yet to be fully addressed is whether the effects seen in individuals exposed to EDCs manifest in measurable changes in population parameters. Whilst some work has been conducted previously investigating the population-level impacts of EDC exposure, this work has generally used mathematical models to examine whether measured short-term changes in individual fecundity and survival may lead to alterations in population viability and growth in the long-term. Such an approach ignores the potential impact of EDCs on more subtle factors (for example alterations in behaviour and genetics) that can potentially affect fish population dynamics. The work presented in this thesis used two model species, the zebrafish, Danio rerio and stickleback, Gasterosteus aculeatus, to examine whether exposure to EDCs had an effect on previously ignored factors that determine group dynamics, including behaviour, parentage and reproductive success. In groups of zebrafish (two males and two females) exposure to the model oestrogenic compound ethinylestradiol (EE2) at 10 ng/L caused a reduction in the paternity success of the most successful male, reducing the skew in paternity, relative to controls. This disruption in the reproductive hierarchy was associated with a suppression of 11-ketotestosterone (11-KT) concentrations in exposed males. Such alterations in reproductive hierarchies have implications for population genetic diversity as well as usual patterns of sexual behaviour and selection. In a second study, males were exposed to EE2 (females were not exposed) and then placed into colonies of varying size with either 1, 2 or 4 males competing to breed with one female. The reproductive success of the most reproductively successful male in colonies containing two males and one female was unaffected by previous exposure to EE2, relative to controls, but was significantly affected for the most reproductively successful male in tanks containing four males competing to breed with one female. This finding suggests that the impact of EDC exposure on reproductive hierarchies and success is dependent on the group structure and is not a straightforward monotonic effect. It is well known that there exist so-called ‘windows of sensitivity’ for the effects of EDCs on sexual development in fish. Exposure to EDCs during this period can cause dramatic alterations in development, including complete sex reversal if the magnitude and/or duration of exposure are sufficient. In the third study in this thesis, zebrafish were exposed during the key window of sexual development, from 20-60 days post fertilisation (dpf). The reproductive success of both mature males and females was then examined in competitive breeding scenarios. Whilst there were no obvious effects of the early life EE2 exposures on the gonadal phenotypes in either males or females at maturity, the reproductive success in males exposed to 2.76ng EE2/L was increased. In contrast, exposure of females to 9.86 ng EE2 /L during early life reduced their subsequent reproductive success. Given the importance of female reproductive capability in population demographics and dynamics, the effect of exposure to EE2 on female reproductive success may therefore have significant implications for exposed fish populations. Whilst conducting the EE2 exposure experiments, it became clear that the genetic diversity in the laboratory strains of zebrafish was much lower than that previously published for wild zebrafish. A study was therefore conducted in which several laboratory strains of zebrafish and a population of zebrafish obtained directly from the wild in Bangladesh were genotyped in order to elucidate the genetic diversity in the different strains. The results showed that the genetic diversity in commonly used laboratory strains (even those described as outbred or ‘wild type’) was significantly lower than that of wild zebrafish. Given the impact of reductions in genetic diversity and variation on fitness at both the individual and population level, this has implications for studies that extrapolate results from laboratory studies to wild populations, as exposure to EDCs may have a different impact on laboratory strains than their more genetically diverse wild counterparts. The final study conducted examined populations of wild sticklebacks (Gasterosteus aculeatus) from either clean sites or sites with a history of exposure to anthropogenic pollutants, particularly EDCs from sewage effluent. All the populations examined from sites with a history of pollutant exposure showed evidence of population bottlenecks, whereas populations from clean sites did not. Fish from the different populations were then placed into competitive breeding mesocosms. Each mesocosm contained an equal number of males from a clean, control reference site and from one of the polluted sites. The same number of females from a clean, control reference site was also added to the mesocosm. Males from all polluted sites were able to compete and breed successfully when placed in these competitive breeding scenarios and there was no evidence that they had reduced reproductive success. The implication of this finding is that even if exposure to anthropogenic EDCs has impacted on the genetics of a wild population, the reproductive potential of individuals may not necessarily be altered.
Please note, for copyright reasons an amended version of the thesis with images removed is available to view and download: CoeT_TPC.pdf
Tyler, Charles R.
PhD in Biological Sciences