Evolutionary and demographic consequences of temperature-induced masculinization under climate warming: the effects of mate choice

Abstract

Background One of the dangers of global climate change to wildlife is distorting sex ratios by temperature-induced sex reversals in populations where sex determination is not exclusively genetic, potentially leading to population collapse and/or sex-determination system transformation. Here we introduce a new concept on how these outcomes may be altered by mate choice if sex-chromosome-linked phenotypic traits allow females to choose between normal and sex-reversed (genetically female) males. Results We developed a theoretical model to investigate if an already existing autosomal allele encoding preference for sex-reversed males would spread and affect demographic and evolutionary processes under climate warming. We found that preference for sex-reversed males (1) more likely spread in ZW/ZZ than in XX/XY sex-determination systems, (2) in populations starting with ZW/ZZ system, it significantly hastened the transitions between different sex-determination systems and maintained more balanced adult sex ratio for longer compared to populations where all females preferred normal males; and (3) in ZW/ZZ systems with low but non-zero viability of WW individuals, a widespread preference for sex-reversed males saved the populations from early extinction. Conclusions Our results suggest that climate change may affect the evolution of mate choice, which in turn may influence the evolution of sex-determination systems, sex ratios, and thereby adaptive potential and population persistence. These findings show that preferences for sex-linked traits have special implications in species with sex reversal, highlighting the need for empirical research on the role of sex reversal in mate choice.

Sex Reversal and Performance in Fitness-Related Traits During Early Life in Agile Frogs

“…In such species, environmental influences can override the effect of genes during sex determination in early life, resulting in sex reversal whereby individuals develop phenotypic sex discordant with their genetic sex (Alho et al, 2010;Baroiller and D'Cotta, 2016;Holleley et al, 2016;Lambert et al, 2019;Nemesházi et al, 2020). Theoretical studies predict that sex reversal has far-reaching consequences for demography, population persistence, sex chromosome loss and evolutionary transitions between sex-determination systems (Grossen et al, 2011;Quinn et al, 2011;Bókony et al, 2017;Wedekind, 2017;Schwanz et al, 2020;Nemesházi et al, 2021). Studying these consequences empirically is especially important in light of the ongoing rapid human-induced environmental alterations, including climate change and chemical pollution, which may increase sex-reversal frequency in nature (Nemesházi et al, 2020).…”

“…Understanding this issue would be highly valuable for at least three reasons. First, it would facilitate forecasting the effects of sex reversal on demography and evolution, because many of these theoretically predicted effects critically depend on the viability and reproductive success of sex-reversed individuals (Grossen et al, 2011;Bókony et al, 2017;Nemesházi et al, 2021). Second, it would provide insight into the ultimate and/or proximate drivers of sex reversal.…”

The significance of biomass allocation to population growth of the invasive species Ambrosia artemisiifolia and Ambrosia trifida with different densities

“…They may adjust their allocation patterns to a given environment in an economical manner [ 6 , 7 ]. This allocation flexibility, in response to environmental variations, is thought to maximise the growth rate or fitness of plants to increase competition [ 8 – 10 ]. In dense populations, plants usually allocate more biomass to aboveground parts, maximising light assimilation and photosynthesis by increasing height [ 11 ].…”

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 Fig S11a,d in Nemesházi et al, 2021a). 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.…”

“…In ectothermic animals, various environmental stimuli can cause a developmental effect rarely seen in endotherms: sex reversal, whereby individuals exposed to such stimuli during their embryonic or larval life-phase develop the sexual phenotype opposite to their genetic sex (Baroiller & D'Cotta, 2016;Flament, 2016;Whiteley, Castelli, Dissanayake, Holleley, & Georges, 2021). Sex reversal occurs in fish, amphibians, and reptiles in nature (Alho, Matsuba, & Merilä, 2010;Baroiller & D'Cotta, 2016;Lambert, Tran, Kilian, Ezaz, & Skelly, 2019;Nemesházi et al, 2020;Whiteley et al, 2021;Xu et al, 2021), and theoretical studies caution that it may have far-reaching consequences including skewed sex ratios, sex-chromosome evolution, and even population extinction (Bókony, Kövér, Nemesházi, Liker, & Székely, 2017;Grossen, Neuenschwander, & Perrin, 2011;Nemesházi, Kövér, & Bókony, 2021;Perrin, 2009;Schwanz, Georges, Holleley, & Sarre, 2020;Wedekind, 2017). Laboratory experiments show that sex reversal can be induced by anthropogenic stressors like chemical pollution and elevated temperature (Flament, 2016;Lambert, Smylie, Roman, Freidenburg, & Skelly, 2018;Mikó et al, 2021;Tamschick et al, 2016), thus, we may expect that the contemporary and future increase in the levels of anthropogenic stressors will influence the rates of sex reversal in freeliving populations of ectothermic vertebrates.…”