Evolution of viviparity in cold-climate lizards: testing the maternal manipulation hypothesis

Abstract

We used a cold-climate viviparous lacertid lizard (Eremias prezwalskii) as a model system to test the maternal manipulation hypothesis. Twenty-four gravid females collected from a population in Inner Mongolia (northern China) were maintained in the laboratory for the whole gestation length, with 12 allowed to bask for 14-h daily and the other 12 for 10-h daily. Females selected lower body temperatures but did not thermoregulate more precisely when gravid. The mean gestation length was shorter in females provided with longer basking opportunity. Neonates in the two treatments differed in tail length and the number of ventral scales but not in other examined morphological traits, with offspring born in the 14-h treatment having longer tails but fewer ventral scales. Offspring were sexually dimorphic at birth, with females being smaller in tail length, head length and fore-limb length but having more ventral scales than males of the same size. Offspring born in the 14-h treatment were not only faster runners but also grew faster than did offspring born in the 10-h treatment. Our data validate the main predictions of the maternal manipulation hypothesis that females should shift selected body temperatures during gestation to provide optimal thermal conditions for developing embryos and that phenotypic traits determined by maternal thermoregulation should enhance offspring fitness. Our study is the first to demonstrate that the maternal manipulation hypothesis applies to cold-climate viviparous reptiles.

Maternal basking regime has complex implications for birthdate and offspring phenotype in a nocturnally foraging, viviparous gecko

“…For example, offspring of Woodworthia 'Otago/ Southland' were proportionately shaped, in contrast with some lizard species in which cool-gestated offspring may have relatively short tails (Shine and Downes, 1999;Li et al, 2009) or relatively small or large mass (Shine and Harlow, 1993;While and Wapstra, 2009). In addition, at 2-3 months of age, geckos from different regimes were able to access a warm retreat as readily and to run by day as quickly.…”

“…However, even under the warmest regime, pregnancies with spontaneous deliveries averaged 178 days (∼6 months), an exceptional length compared with that in diurnal lizards with similar-sized offspring and similar basking opportunity (∼51-71 days; Beuchat, 1988;Schwarzkopf and Shine, 1991;Li et al, 2009). Under the cool regime, mean gestation length in geckos increased by 25% (to 223 days), a smaller difference than might be expected given that basking opportunity was reduced by 50%.…”

“…However, among spontaneously delivered offspring, those from the cool regime were small (in SVL) and slowgrowing (in mass). Small size and/or slow subsequent growth have sometimes been seen in offspring of diurnal lizards from cool maternal regimes (Swain and Jones, 2000;Wapstra, 2000;Li et al, 2009), though not always (e.g. patterns can vary between populations: Caley and Schwarzkopf, 2004;Cadby et al, 2014).…”

“…In addition, at 2-3 months of age, geckos from different regimes were able to access a warm retreat as readily and to run by day as quickly. Among other viviparous lizards, effects of a low maternal basking regime on offspring speed appear variable: neonates may be relatively slow (While et al, 2009a;Li et al, 2009), relatively fast (Shine and Harlow, 1993;Swain and Jones, 2000) or show no difference (Shine and Downes, 1999), and differences may disappear within 2-3 months (Swain and Jones, 2000;Hare and Cree, 2010). In Woodworthia 'Otago/Southland', the faster mean speed by day at 25°C than at night at 15°C is attributable to the effect of temperature rather than photoperiod: in adults of this species, sprint speed does not vary between day and night at constant temperature, whereas sprint speed varies by day between 25 and 15°C (Gaby et al, 2011).…”

“…Additionally, although reduced thermal opportunity during pregnancy often increases gestation length in lizards, consistent effects on offspring running speed and/or size are not apparent (e.g. Ji et al, 2006;Li et al, 2009;Cadby et al, 2014), and for a skink with asynchronous births, differences in running speed between first-and last-born offspring within a litter were not consistent across the birth season (While et al, 2009a). Extended gestation or delayed parturition can also have negative consequences (e.g.…”