Podocnemis expansa Turtles Hint to a Unifying Explanation for the Evolution of Temperature-Dependent Sex Determination in Long-Lived and Short-Lived Vertebrates

Abstract

The adaptive significance of temperature-dependent sex determination (TSD) remains elusive for many long-lived reptiles. Various hypotheses proposed potential ecological drivers of TSD. The Charnov-Bull’77 model remains the most robust and explains the maintenance of TSD in short-lived vertebrates, where sex ratios correlate with seasonal temperatures within years that confer sex-specific fitness (colder springs produce females who grow larger and gain in fecundity, whereas warmer summers produce males who mature at smaller size). Yet, evidence of fitness differentials correlated with incubation temperature is scarce for long-lived taxa. Here, it is proposed that the Charnov-Bull’77 model applies similarly to long-lived taxa, but at a longer temporal scale, by revisiting ecological and genetic data from the long-lived turtle <i>Podocnemis expansa</i>. After ruling out multiple alternatives, it is hypothesized that warmer-drier years overproduce females and correlate with optimal resource availability in the flood plains, benefitting daughters more than sons, whereas resources are scarcer (due to reduced flowering/fruiting) during colder-rainier years that overproduce males, whose fitness is less impacted by slower growth rates. New technical advances and collaborative interdisciplinary efforts are delineated that should facilitate testing this hypothesis directly, illuminating the understanding of TSD evolution in <i>P. expansa</i> and other long-lived TSD reptiles.

Differential early‐life survival underlies the adaptive significance of temperature‐dependent sex determination in a long‐lived reptile

“…It is thought that TSD evolved independently across different taxonomic groups and likely represents a convergent outcome stemming from different selective pressures (Janzen & Phillips, 2006; Sarre et al, 2011; Valenzuela & Lance, 2004). In contrast to the findings reported here in which incubation temperature affects survivorship, TSD in jacky dragons likely arose due to incubation temperature‐driven variation in body size and consequent reproductive success (Warner & Shine, 2007, 2008).…”

“…Beyond challenges associated with measuring components of fitness for long‐lived species in the field, seasonal effects on offspring growth like those observed in the silverside and jacky dragon are unlikely to translate into differences in reproductive performance when individuals do not reach maturity for several years or even decades. This may indicate that TSD is adaptively neutral in these cases (Sabath et al, 2016; Valenzuela & Lance, 2004) or that adult fecundity is not the relevant target of selection (Sæther et al, 2013). Effects of the developmental environment on the other key component of fitness, survival, have received comparatively less attention.…”

Transcriptomic thermal plasticity underlying gonadal development in a turtle with ZZ/ZW sex chromosomes despite canalized genotypic sex determination

“…Temperature‐dependent sex determination predominates in turtles and is the likely ancestral state from which GSD evolved multiple times independently as XX/XY or ZZ/ZW systems of sex chromosomes (Bista & Valenzuela, 2020; Janzen & Krenz, 2004; Organ & Janes, 2008; Sabath et al, 2016), which may have been lost in some turtle lineages that reverted back to TSD (Literman et al, 2018; Valenzuela & Adams, 2011). Whether TSD is adaptive in turtles remains the focus of theoretical and empirical research (Schwanz & Georges, 2021; Valenzuela, 2021) as does the evolution of turtle sex chromosomes and their dosage compensation (Bista et al, 2021; Bista & Valenzuela, 2020; Rovatsos & Kratochvíl, 2021). In TSD turtles, the incubation temperatures experienced by the embryo around the middle third of development determine whether the bipotential gonads develop into testes or ovaries by influencing molecular and cellular processes (Merchant‐Larios et al, 2021).…”

Sex determination and optimal development in the Moorish gecko, Tarentola mauritanica

“…Under environmental sex determination (ESD), sex is established in response to a nongenetic factor experienced within a discrete period after fertilization (Bull, 1983). Within ESD, temperature sex determination (TSD) is a special case where the sex of progeny is determined by the temperature experienced during their embryonic development (Bull, 1980;Janzen & Paukstis, 1991;Valenzuela & Lance, 2004). Among reptiles, all crocodilians and sphenodontians have exclusively TSD, whereas squamates and turtles can exhibit either TSD or genetic sex determination (GSD) (Janzen & Phillips, 2006;Sabath et al, 2016) with a few species combining both (e.g.…”