Sex reversal and ontogeny under climate change and chemical pollution: are there interactions between the effects of elevated temperature and a xenoestrogen on early development in agile frogs?

Abstract

Anthropogenic environmental change poses a special threat to species in which genetic sex determination can be overwritten by the thermal and chemical environment. Endocrine disrupting chemicals as well as extreme temperatures can induce sex reversal in such species, with wide-ranging consequences for fitness, demography, population viability and evolution. Despite accumulating evidence suggesting that chemical and thermal effects may interact in ecological contexts, little is known about their combined effects on sex reversal. Here we assessed the simultaneous effects of high temperature (masculinizing agent) and 17α-ethinylestradiol (EE2), a widespread xenoestrogen (feminizing agent), on sexual development and fitness-related traits in agile frogs (Rana dalmatina). We exposed tadpoles to a six-days heat wave (30°C) and/or an ecologically relevant concentration of EE2 (30 ng/L) in one of three consecutive larval periods, and diagnosed sex reversals two months after metamorphosis using species-specific markers for genetic sexing. We found that high temperature induced female-to-male sex reversal, decreased survival, delayed metamorphosis, decreased body mass at metamorphosis, and increased the proportion of animals that had no fat bodies, while EE2 had no effect on these traits. Simultaneous exposure to heat and EE2 had non-additive effects on juvenile body mass, which were dependent on treatment timing and further complicated by a negative effect of sex reversal on body mass. These results show that environmentally relevant exposure to EE2 does not diminish the masculinizing effects of high temperature. Instead, our findings on growth suggest that climate change and chemical pollution may have complex consequences for individual fitness and population persistence in species with environment-sensitive sex determination.

Effects of chlorpyrifos on early development and anti-predator behavior of agile frogs

“…Thus, it seems that the ecologically relevant concentrations that we used are not harmful for sexual development in agile frogs. A low incidence of intersexuality may be a natural phenomenon in young postmetamorphic amphibians (Orton and Tyler, 2015), and is in accordance with the rare occurrence of spontaneous sex reversal we found in agile frogs (Mikó et al, 2021;Nemesházi et al, 2020).…”

“Heat waves” experienced during larval life have species-specific consequences on life-history traits and sexual development in anuran amphibians

“…This resulted in nine treatments with 48 replicates (4 individuals per family × 12 families) in each treatment for each species. In agile frogs, data from the 19 and 30 °C treatments presented here were also used (combined with data from additional treatment groups) for testing another a-priori study question, which we published elsewhere (Mikó et al 2021). We performed thermal treatments in a separate room adjacent to the room where we reared tadpoles.…”

“…Also, though amphibian larvae generally exhibit a relatively high thermal tolerance (Ultsch et al 1999, Sunday et al 2011, but also see Harkey and Semlitsch 1988, Wallace and Wallace 2000, Bellakhal et al 2014, Goldstein et al 2017 temperatures as low as 30 °C experienced during the larval period can be detrimental to them. Heat can result in delayed metamorphosis (Goldstein et al 2017), reduced body mass (Harkey and Semlitsch 1988, Phuge 2017, Lambert et al 2018, disabled locomotor activity (Goldstein et al 2017), sex reversal (Dournon et al 1984, Wallace and Wallace 2000, Mikó et al 2021) and biased sex ratios (Phuge 2017, Lambert et al 2018, Ruiz-Garciá et al 2021. Exposure of adult frogs to 30 °C or higher can increase stress hormone levels (Juráni et al 1973, Narayan andHero 2014) and enhance the processes that contribute to accelerated ageing (Burraco et al 2020).…”

“…However, we still know little about the developmental costs of brief periods of high temperatures for larval amphibians because most experiments that investigated the effects of heat on larval fitness exposed animals to heat chronically for several weeks, and the effects of shorter heat pulses are rarely tested (Mikó et al 2021). Because the effects of high temperatures are likely to depend on the intensity, timing and duration of exposure, and may differ between species, studies focusing on these sources of variation are necessary to assess potential malign impacts of heat waves on amphibians and uncover hidden risks arising from thermal treatment of diseased animals.…”

Novel genetic sex markers reveal unexpected lack of, and similar susceptibility to, sex reversal in free‐living common toads in both natural and anthropogenic habitats

“…Due to their sex‐chromosome genotype, sex‐reversed individuals may be unable to produce daughters or sons (Wedekind, 2017), and therefore may be selected against by sex‐ratio selection (Schwanz & Georges, 2021; see also figure a,d in Nemesházi, Kövér, et al, 2021). Also, sex‐reversed individuals may perform poorly in traits that influence survival (Mikó et al, 2021; Nemesházi et al, 2020) or sexually selected traits (Nemesházi, Kövér, et al, 2021). In such situations, we can expect resistance to sex reversal to be adaptive in environments where sex‐reversing stressors are pervasive.…”