INTRODUCTION:
In oviparous vertebrates, maternal provisioning of nutrients and signaling molecules is critical for proper development and can be a major determinant of offspring traits (Groothuis et al., 2005; Radder et al., 2007; Van Dyke and Griffith, 2018). Complex biological and ecological factors, including maternal diet (Royle et al., 2003; Warner and Lovern, 2014), stress (McCormick, 1998; Saino et al., 2005), and age (Beamonte‐Barrientos et al., 2010; Urvik et al., 2018) can influence the quantity and quality of resources provisioned to embryos (Moore et al., 2019; Mousseau and Fox, 1998). In addition, components of the developmental environment can influence how maternal resources are utilized by developing embryos (Brown et al., 2011; Du and Shine, 2022, 2008; Mueller et al., 2015; Shine and Brown, 2002). For example, egg mass is a primary determinant of hatchling mass (Deeming and Birchard, 2007), but incubation temperature has been shown to modify the efficiency by which maternal resources are converted into somatic tissue (Bock et al., 2021; Marshall et al., 2020; Pettersen et al., 2019) and how those resources are allocated to different phenotypes (Flatt, 2001; Telemeco et al., 2010). However, despite the importance of maternal provisioning and incubation temperature in shaping hatchling phenotypes, the extent to which these factors contribute to trait variation across populations is not well resolved (but see (Bodensteiner et al., 2019; Orizaola and Laurila, 2016, 2009; Richter‐Boix et al., 2015)).
Species with broad geographic ranges are likely under selective pressures to maximize fitness under population-specific ecological conditions, which can include altering embryonic responses to maternal resources and environmental variables (Conover and Schultz, 1995; Kawecki and Ebert, 2004; Merilä et al., 2000; Orizaola and Laurila, 2009). For instance, in oviparous reptiles, latitudinal differences in the influence of temperature on incubation duration have been shown to occur across populations (Du et al., 2010a; Pettersen, 2020). Whereas cooler incubation temperatures slow development, populations from northern latitudes often show counter-gradient variation in incubation duration, developing faster than populations from more southern latitudes at the same temperatures (Pettersen, 2020). Similarly, high altitude populations of wall lizards (Podacris uralis ) have been shown to allocate more maternal resources towards somatic tissue relative to low altitude populations when raised at a common temperature (Pettersen et al., 2023). However, the extent to which populations vary in how maternal provisioning and incubation temperature shape additional fitness-related traits in taxonomically diverse species remains unclear. Such information is critical to understand how responses to developmental conditions contribute to adaptive evolutionary change.
In the present study, we test whether embryonic responses to maternal provisioning and incubation temperature show interpopulation variation by examining several fitness-related traits in a large reptile, the American alligator (Alligator mississippiensis ). Like many turtles and some lizards, crocodilians display temperature-dependent sex determination (TSD), in which thermal signals experienced during a discreet developmental window determine sex, along with additional phenotypic traits (Allsteadt and Lang, 1995; Bock et al., 2021; Kohno et al., 2014; McCoy et al., 2016): incubations at warmer, male-promoting temperatures (MPT) result in larger hatchlings with greater residual yolk reserves than those incubated at female-promoting temperatures (FPT). Recent reports demonstrate that temperature sensitive traits, including body mass index (BMI) and snout-vent length (SVL), correlate with juvenile survival in this species (Bock et al. 2023, preprint; Johnson et al. 2023), which may contribute to the adaptive significance of TSD (Schwanz et al. 2016; Bock et al. 2023, preprint). This life history strategy, combined with the unique taxonomic position of crocodilians relative to other extant vertebrates, makes alligators particularly informative in deciphering how variation in response to the developmental environment contributes to trait diversity across populations. The alligator’s range extends from southern Florida to northeastern North Carolina, providing ample opportunity for local adaptation of phenotypic responses to maternal resources and incubation temperature. Yet, the extent to which embryonic response to these components of the developmental environment vary across populations is currently unknown. Here, we use a common garden incubation and grow out design to resolve the relative influence of egg mass (a proxy for maternal provisioning) and incubation temperature on morphological and metabolic traits across two northern and two southern populations spanning a large latitudinal portion of the alligator’s geographic range.