How fish eggs are preadapted for the evolution of matrotrophy

Abstract

Teleost fishes evolved livebearing via egg retention 14 times. Matrotrophy has evolved within 12 of those lineages. By contrast, squamate reptiles evolved livebearing over 115 times, but only two to four of those lineages are known to have evolved matrotrophy. Is the discrepancy between these organisms in the probability of this transition caused by differences in their eggs? We show that the eggs of oviparous species in the superorder Atherinomorpha can acquire small organic molecules from their surrounding environment against a concentration gradient via mechanisms of active transport. Uptake rates were inhibited by competing radiolabelled amino acids against unlabelled versions of themselves. Transport was non-specific as uptake rates were similar for l -leucine and its biologically uncommon enantiomer d -leucine. Eggs are also capable of transporting larger microspheres across the membrane, but transport is inhibited at temperatures below 4°C, suggesting active transport occurs via pinocytosis. Conflict theory predicts that the ability of the egg to acquire maternal resources will facilitate the embryo–parent arms race that leads to the evolution of matrotrophy following the transition to livebearing. The shelled eggs of amniotes lack such access to maternal resources when retained in the evolution of viviparity.