"Grandfather Effects": The Genetics of Interpopulation Differences in Offspring Size in the Mosquito Fish

Abstract

There is a greater than 2-fold difference in offspring weight between populations of the mosquito fish G. affinis, an ovoviviparous poeciliid. This study determined if these differences have a genetic basis. The hybridization of virgin F1 offspring from 2 localities revealed a large maternal, but no paternal, contribution to offspring size. The backcross of virgin F2 females to wildcaught males demonstrated a significant grandfather effect. An F1 male from a locality that produces relatively large offspring caused an increase in the size of F3 offspring. The weight of an offspring is evidently determined by the maternal genotype, rather than its own genotype. The paternal (F1) genetic contribution is therefore not seen in F2 offspring, but, because he contributes to the genotype of F2 females, is seen in the size of F3 offspring. The proposed underlying mechanism for a similar case of delayed inheritance, the direction of shell coiling in the snail Limnaea peregra, provides a clue to why Gambusia display this pattern. The direction of shell coiling appears to be determined by the plane of the 1st cleavage, prior to the expression of the paternal genome. Similarly, offspring weight appears to be determined prior to fertilization in these Gambusia. In the 4 populations surveyed, embryo weight is greatest in the earliest stages of development, and declines by an average of 36.3% over the course of development. The ova maybe fully provisioned prior to fertilization, with little or no input by the female after fertilization. The paternal genome thus has little opportunity to have an impact on offspring weight at birth. Delayed inheritance for offspring size should be the rule in all egg laying and ovoviviparous organisms. Because many aspects of life histories are correlated with offspring weight, establishing a genetic basis for these variables may require 2 generation experiments.