Abstract
The evolution of matrotrophy (post-fertilization maternal provisioning to developing embryos) has been explained through several hypotheses. Trexler and DeAngelis proposed in 2003 a theoretical model that defines the ecological conditions under which matrotrophy would be favored over lecithotrophy (pre-fertilization maternal provisioning). According to this model, matrotrophy offers a selective advantage in environments with abundant and constantly available food, whereas environments with limited and fluctuating food resources should instead promote a lecithotrophic mode of maternal provisioning. This model also proposes that matrotrophy entails the consequence of leaner reproductive females and in turn shorter lifespans. In this study, we examined the Trexler-DeAngelis model using data from 45 populations of five viviparous species from the fish genus Poeciliopsis (family Poeciliidae). We used the matrotrophy index (MI) as a measure of post-fertilization maternal provisioning, and the index of stomach fullness and individual body condition (BC) as proxies for food availability. We also estimated the magnitude of fluctuations in food availability by calculating the temporal variances of these two proxies. Neither abundant nor constantly available food were associated with greater degrees of matrotrophy, which fails to support the predictions of the Trexler-DeAngelis model with respect to the ecological drivers of increased post-fertilization provisioning to embryos. Nonetheless, in all five species we observed that females with greater degrees of matrotrophy had poorer BC compared to females that provided less nutrients to embryos after fertilization. This finding is consistent with one of the expected consequences of advanced matrotrophy according to the Trexler-DeAngelis model, namely, a detriment to the nutritional status of females. Our study provides compelling evidence that gestating females experience a trade-off between post-fertilization provisioning to embryos and self-maintenance, revealing in turn that matrotrophy is a costly reproductive strategy.
Highlights
Viviparity is a reproductive strategy in which the embryo develops inside a specialized structure or cavity within the female after fertilization (Blackburn, 1999)
We focused on five species of the genus Poeciliopsis with relatively wide geographic distributions, which allowed us to examine interpopulation differences in food availability and how such differences affect the patterns of embryo nourishment
We used the index of stomach fullness (IF), which was calculated for each female as the dry mass of her digestive tract divided by her somatic dry mass, and multiplying the result by 100 (Hyslop, 1980)
Summary
Viviparity is a reproductive strategy in which the embryo develops inside a specialized structure or cavity within the female after fertilization (Blackburn, 1999). This reproductive strategy can be found in mammals, sharks, anurans, salamanders, snakes, lizards, and fishes (Shine and Bull, 1979; Guillette and Jones, 1985; Greven and Guex, 1994; Castro, 2009; Renfree et al, 2013; Wake, 2015). The first mechanism is lecithotrophy, in which the mother transfers all nutrients to her embryos before fertilization in the form of yolk and does not transfer additional resources during their development (Blackburn, 1992). The second mechanism is matrotrophy, which unlike lecithotrophy, involves the continuous provisioning of nutrients from the mother to the developing embryos after fertilization, usually through specialized structures (e.g., placentas; Wourms, 1981; Lombardi and Wourms, 1985; Blackburn, 1992; Marsh-Matthews, 2011; Kwan et al, 2015; Olivera-Tlahuel et al, 2019)
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