Effects of Maternal Basking and Food Quantity during Gestation Provide Evidence for the Selective Advantage of Matrotrophy in a Viviparous Lizard

Abstract

The evolution of matrotrophy (i.e., direct supply of nutrients by the mother during gestation) may be associated with high maternal energy availability during gestation. However, we lack knowledge about the selective advantages of matrotrophic viviparity (live-bearing) in reptiles. In reptiles, the interaction between body temperature and food intake affect maternal net energy gain. In the present study, we examined the effects of basking and food availability (2 by 2 factorial design) during gestation on offspring phenotype in a matrotrophic viviparous lizard (Pseudemoia entrecasteauxii). Subsequently, we investigated if the maternal effects were context-dependent using offspring growth rate as an indicator of the adaptive significance of matrotrophy. Offspring were exposed either to the same thermal conditions as their mothers experienced or to thermal conditions different from those experienced by their mothers. We provide the first evidence that an interaction between maternal thermal and maternal food conditions during gestation strongly affects offspring phenotype, including date of birth, body size and performance ability, which affect offspring fitness. Offspring growth rate was dependent on offspring thermal conditions, but was not influenced by maternal effects or offspring sex. Matrotrophic viviparity provided gravid females with the means to enhance offspring fitness through greater energetic input to offspring when conditions allowed it (i.e., extended basking opportunity with high food availability). Therefore, we suggest that selective advantages of matrotrophic viviparity in P. entrecasteauxii may be associated with high maternal energy availability during gestation.

High Food Abundance Permits the Evolution of Placentotrophy: Evidence from a Placental Lizard,Pseudemoia entrecasteauxii

“…Thus, previous measurements of matrotrophy index, which were calculated from captive females with abundant food (e.g., Stewart and Thompson 1993;Thompson et al 1999bThompson et al , 2001, may not be representative of placentotrophy in wild populations. Instead, individuals likely vary widely in placentotrophic provisioning depending on their foraging success (and body temperature; Itonaga et al 2012b) during gestation. Our data clearly show that differences in offspring size due to differing feeding regimes in placentotrophic skinks (e.g., Shine and Downes 1999;Itonaga et al 2012b) are caused by differences in placental transport of protein, lipid, and energy during gestation.…”

“…Instead, individuals likely vary widely in placentotrophic provisioning depending on their foraging success (and body temperature; Itonaga et al 2012b) during gestation. Our data clearly show that differences in offspring size due to differing feeding regimes in placentotrophic skinks (e.g., Shine and Downes 1999;Itonaga et al 2012b) are caused by differences in placental transport of protein, lipid, and energy during gestation. In particular, offspring from high-food treatments contained nearly twice as much protein as did freshly ovulated eggs.…”

“…The latter explanation seems unlikely given the high rates of abortion and cannibalism we observed when food was limited. Furthermore, pregnant female P. entrecasteauxii are more likely to retain nutrients when highly stressed and allocate more nutrients to offspring when less stressed, regardless of food abundance (Itonaga et al 2012a). Thus, we suggest that parent-offspring conflict occurs in P. entrecasteauxii, with embryos exerting some control over maternal provisioning and mothers ultimately reclaiming those nutrients from poor-quality offspring via cannibalism if food becomes scarce.…”

Viviparous placentotrophy in reptiles and the parent–offspring conflict

“…Placental structure, function, and development have been studied in detail in Pseudemoia (Stewart and Thompson, , ; Adams et al, ; for summaries, see Stewart and Thompson, ; Stewart and Blackburn, ). At least three of the six species are modestly placentotrophic, and the amount of nutrient transfer is facultatively regulated (Thompson et al, , , ; Itonaga et al, , ; van Dyke et al, 2014a). Despite modest differences in the degree of placentotrophy, placentation is similar in the studied species, at least at the level of light microscopy.…”

Maternal food availability affects offspring performance and survival in a viviparous lizard

“…Although various studies attempt to identify the adaptive significance of maternal effects in diverse organisms, from plants to invertebrates to vertebrates (Galloway ; Steiger et al . ; Donelson, Mccormick & Munday ; Itonaga, Jones & Wapstra ; Araminaite et al . ; Henderson et al .…”