How individuals allocate resources to different biological functions such as maintenance, somatic growth and reproduction is crucial for their life-history (Stearns, 1992). Different functions compete for limited resources, leading to trade-offs and a limited set of possible life-history strategies (Braendle et al., 2011).

In addition to intrinsic trade-offs and constraints, resource allocation and hence life-histories are also influenced by environmental factors, such as food availability (Boggs, 1992; Santi et al., 2020). Increased maternal food availability enables a higher energy uptake, which can be allocated to any function (van Noordwijk and de Jong, 1986). However, when food is scarce, specific functions may be prioritized over others. In lecithotrophic live-bearing animals, where all resources are allocated to the eggs prior to fertilization, adverse food conditions may reduce maternal growth, fat reserves and fecundity (Bashey, 2008; Reznick et al., 1996; Wang et al., 2017), yet also increase the relative investment in offspring size (Bashey, 2008; Reznick et al., 1996). In this example, mothers adaptively modified offspring phenotype in preparation for predicted, adverse environmental conditions (low food availability). This response is presumably advantageous, as under competitive adverse food conditions, mothers gain fitness benefits by producing larger offspring (Leips et al., 2013; Parker and Begon, 1986). However, as optimal offspring size is given by the offspring size–performance relationship, which depends on the environment, the advantage of producing larger offspring at birth diminishes or disappears in favourable environments (Bashey, 2008; Leips et al., 2013; Parker and Begon, 1986), and the predicted optimal strategy for the mother is to produce more numerous but smaller offspring (Jørgensen et al., 2011). If the maternal environment reliably predicts future environmental conditions, females may evolve the ability to adaptively adjust offspring phenotype at birth, based on environmental cues (Mousseau and Fox, 1998a).

The modulation and timing of nutrient acquisition and allocation also affect life-histories (Zera and Harshman, 2001). In matrotrophic live-bearing animals, experimental manipulations of food availability can impact the pattern of resource allocation to offspring (Banet and Reznick, 2008; Banet et al., 2010; Pollux and Reznick, 2011; Reznick et al., 1996; Van Dyke and Griffith, 2018). Instead of allocating all resources to the eggs prior to fertilization (i.e. lecithotrophy), matrotrophic species transfer nutrients to their embryos throughout gestation via a placenta (Pollux et al., 2014; Reznick et al., 2002; Wourms, 1981). Because matrotrophic species continuously supply embryos with resources, determination of brood size (i.e. number of embryos per brood) and offspring size are decoupled (Pollux and Reznick, 2011). When resource conditions during pregnancy suddenly deteriorate, matrotrophic species may not be able to optimally provision their embryos. Because females cannot abort embryos in response to food shortage and maternal fat reserves do not fully buffer females during gestation (Banet and Reznick, 2008; Banet et al., 2010; Pollux and Reznick, 2011; Reznick et al., 1996), sudden resource declines inevitably result in smaller, worse-conditioned (i.e. having lower fat reserves) offspring at birth. Small offspring size in low food conditions is associated with a lower survival (Bashey, 2008; Leips et al., 2013; Parker and Begon, 1986). Therefore, matrotrophy has been argued to be maladaptive in fluctuating resource environments (Pollux and Reznick, 2011; Reznick et al., 1996; Trexler and DeAngelis, 2003).

Differential resource allocation to offspring size at birth can impact postnatal development and survival (Mousseau and Fox, 1998b). In fish, body size is linked to locomotor performance (Gibb et al., 2006). Smaller offspring are likely to perform worse on fast-start escapes (Dial et al., 2016), presumably decreasing survival probability in environments with high predation risks. Prey-capture abilities immediately after birth also heavily depend on swimming performance. Newborn live-bearing fish are super-precocial, having functional prey-capture abilities at birth and relying on active exogenous feeding after birth (Lankheet et al., 2016). Moreover, they rapidly develop the visuo-motor skills required for prey capture during the first days after birth and effectively improve their success rate, promoting food uptake and survival (Lankheet et al., 2016). Offspring size thus affects locomotor performance and prey-capturing abilities after birth. However, it is still unknown to what extent restricted maternal food availability during pregnancy affects offspring swimming performance in fast-start escapes and in prey capture after birth.

Here, we examine the effects of maternal food restriction during pregnancy on growth and locomotor performance of offspring after birth in the matrotrophic fish species Phalloptychus januarius Hensel 1868 (family Poeciliidae). If matrotrophy is maladaptive under these circumstances, one may expect differences in offspring size as well as locomotor performance. Specifically, we measured: (i) size and body fat of offspring at different ages (i.e. 0 and 7 days), (ii) fast-start escape performance at birth, and (iii) swimming kinematics while feeding during the first week after birth, to quantify immediate and early postnatal effects of food restriction during pregnancy on offspring size, quality, and locomotor performance. As a proxy for locomotor performance, we focused on mean and maximum speed and acceleration of fast starts and feeding actions. By combining the different measurements, we reveal consequences of maternal food restriction for life-history variation and its implications for the quality and performance of newborn fish in a placental species.