Do female newts modify thermoregulatory behavior to manipulate egg size?

Highlights

• Female ectotherms affect offspring phenotypes by their thermoregulatory behavior.

• We examined the influence of maternal thermoregulation on egg size in newts.

• Reproductive females maintained less variable body temperatures than nonreproductive.

• Maternal thermal requirements had no effect on egg size and early cleavage rate.

• Newts do not manipulate egg traits by maternal thermoregulation.

Abstract

Reproductive females manipulate offspring phenotypes by modifying conditions during embryogenesis. In ectotherms, the environmental control over embryogenesis is often realized by changes in maternal thermoregulation during gravidity. To determine if reproduction influences thermoregulatory behavior in species where females lay eggs shortly after fertilization (strict oviparity), we compared preferred body temperatures (T_p) between reproductive (egg-laying) and non-reproductive female newts, Ichthyosaura alpestris. Next, we exposed reproductive females to temperatures mimicking T_p ranges of reproductive and non-reproductive individuals to find out whether the maternally modified thermal regime influences ovum and jelly coat volume, and early cleavage rates at the time of oviposition. In the thermal gradient, reproductive females maintained their body temperatures within a narrower range than non-reproductive individuals. The exposure of ovipositing females to temperatures preferred during their reproductive and non-reproductive period had a negligible influence on egg size and early cleavage rates. We conclude that the modification of maternal thermoregulatory behavior provides a limited opportunity to manipulate egg traits in newts.

Introduction

Mothers affect their offsprings’ phenotype not only via genes but also with environmental conditions during embryonic development (maternal effect). Countless studies have demonstrated that maternally-manipulated environments benefit developing embryos (Lorioux et al., 2013, Madsen and Shine, 1999, Rieger et al., 2004). On the other hand, females can also behave in the opposite way, i.e. by providing detrimental conditions for individual offspring (Gripenberg et al., 2007, Rosenheim et al., 2008, Scheirs et al., 2000). Current conceptual advances in maternal effect studies resolved this paradox by viewing the adaptive maternal effect from the female rather than offspring’s lifetime reproductive success (Marshall and Uller, 2007). From this view, maternally-provided conditions may be beneficial, neutral, or even detrimental to developing embryos. Despite the conceptual progress in this field, benefits of some maternal behaviors remain unclear.

In many ectotherm taxa, gravid females often modify the mean or variance in body temperatures that benefit her offspring (Shine and Downes, 1999; Mathies and Andrews, 1997, Rodriguez-Díaz and Braña, 2011). Originally, the thermoregulatory shift was explained as a solution to the conflict between disparate thermal optima for mother and offspring phenotypes (Beuchat and Ellner, 1987). In agreement with the current view (see above), it has been recently proposed that maternal thermoregulation may favor not only offspring survival, the maternal manipulation hypothesis (Shine, 1995), but also female performance (Schwarzkopf and Andrews, 2012). However, because females of most examined taxa, squamate reptiles, deposit their eggs in later developmental stages (stages 30–40 after Dufaure and Hubert, 1961), determining whether maternal thermoregulatory behavior primarily increases female performance or offspring survival seems a challenging task. One previously omitted solution to the ‘chicken and egg’ problem is the focus on maternal thermoregulation in non-squamate taxa with the most primitive reproductive mode, when a female oviposits shortly before or after fertilization (strict oviparity). If strictly oviparous females modify their thermoregulatory behavior during reproduction, it clearly shows that maternal thermoregulatory adjustments evolved primarily for other reasons than the manipulation of offspring phenotypes.

Among the few studies on non-squamate systems examining the influence of reproduction on preferred body temperatures (T_p; Gvoždík, 2005, Webber et al., 2015), tailed amphibians, newts, seem particularly suitable for this task. Reproductive females of the Italian crested newt, Triturus carnifex, modified both their T_p mean and range relative to their non-reproductive counterparts (Gvoždík, 2005). Newts are strictly oviparous species and their eggs are laid before or shortly after the first cleavage (Griffiths and de Wijer, 1994). Accordingly, fertilized eggs stay in the oviduct for 4.5–12 h depending on temperature (Epperlein and Junginger, 1982, Bonacci et al., 2005). In contrast, newt embryonic development lasts about 15 days under thermally fluctuating conditions (Měráková and Gvoždík, 2009), and thus maternal thermoregulatory behavior provides a negligible opportunity for maternal thermal manipulation of offspring phenotypes during embryonic development. However, female body temperatures affect ovum size (Kaplan, 1987), and thereby offspring fitness-related traits, in amphibians (Bernardo, 1996, Kaplan, 1980, Semlitsch and Gibbons, 1990). Hence, newt maternal thermoregulation may affect offspring phenotypes in this previously unexplored way. In addition, because temperature influences most functions and processes within an organism (Cossins and Bowler, 1987), it may also modify the production of egg jelly coats. The jelly coating has many functions ranging from fertilization to protection (Shu et al., 2015), and thus their volume surrounding the oocyte is potentially adaptive. Whether maternally-modified temperatures affect newt ovum or jelly coat size is unknown.

In this study, we examined if reproductive alpine newt females, Ichthyosaura alpestris, modify egg size and early cleavage rates by modifying their thermoregulatory behavior. We expect that in strictly oviparous ectotherms, i.e. not carrying embryos in their bodies, the only possibility to effectively manipulate offspring phenotypes through maternal thermoregulatory behavior is via its effect on egg traits. Our aim was twofold. First, we tested the influence of reproductive state on T_p in female newts. Second, we exposed reproductive female newts to temperatures mimicking T_p ranges of reproductive and non-reproductive females to determine whether various thermal regimes affect the size and early cleavage rate of their eggs.