Insulin‐like growth factor 1 and life‐history evolution of passerine birds

Abstract

Natural selection has generated a diversity of ways in which vertebrates allocate their resources between fundamental life‐history traits. The availability of possible evolutionary trajectories of these traits is limited by various genetic, physiological and phylogenetic constraints. This causes trade‐offs due to shared resource pools for, or genetic linkage of, competing traits. The majority of these trade‐offs are mediated by hormones and create the variability in phenotypes that can be observed in nature. Insulin‐like growth factor 1 (IGF‐1) is an evolutionarily conserved peptide, which has been shown to be essential in the regulation of body size, the pattern of reproductive investment and life span across a broad taxonomic range of model species in laboratory and domesticated conditions. However, studies addressing corresponding evolutionary hypotheses on a broader scale and in free‐living vertebrates are very rare. In this phylogenetic comparative study on free‐living passerines (Passeriformes), we explore the way in which plasma IGF‐1 levels underlie the evolution of body size and demographic fitness correlates (clutch size, egg weight, life span). We showed firstly that IGF‐1 levels were positively associated with the body size of passerines, although smaller birds had larger IGF‐1‐mediated investment into building up their body faster. IGF‐1 levels were negatively associated with life span of passerines, and more so in birds with smaller body weight. Finally, IGF‐1 levels were negatively associated with clutch size in heavier species, and positively associated with egg weight in species with higher body weight and longer duration of parental care. The pattern was opposite in species with smaller body weight and shorter duration of parental care. The described evolutionary framework indicates that variation in IGF‐1 levels can be regarded as an important mechanism that may underlie life‐history evolution in passerines. IGF‐1 could act as a physiological link mediating the inter‐regulatory growth–reproduction–lifespan “life‐history triangle” on the pace‐of‐life continuum. Interestingly, body weight and investment into parental care have likely imposed a constraining effect on the IGF‐1‐mediated co‐evolution of demographic fitness traits, such as life span or reproductive investment. This has limited the availability of adaptive pathways via which those traits could evolve as passerines diversified. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.12993/suppinfo is available for this article.

The Relationship between Hormones, Glucose, and Oxidative Damage Is Condition and Stress Dependent in a Free-Living Passerine Bird

“…Similarly, IGF-1 decreased after 180 min or 24 h of confinement in rainbow trout (Oncorhynchus mykiss) and Atlantic salmon (Salmo salar), respectively (Wilkinson et al 2006). In contrast, IGF-1 stayed relatively stable up to 34 min in some passerine birds (Lodjak et al 2018). These results suggest that the stress sensitivity of IGF-1 may vary across species and/or life-history stages and therefore should be accounted for in future studies involving free-living nonmodel organisms in which sampling time usually exceeds 3 min.…”

Dietary restriction and insulin‐like signalling pathways as adaptive plasticity: A synthesis and re‐evaluation

“…Comparative studies have documented interesting relationships between circulating IGF-1 levels and life-history variation across species of birds and mammals (Lodjak, Mänd, & Mägi, 2018;Swanson & Dantzer, 2014). Measurement of IGF-1 in samples collected as part of individual-based studies of wild vertebrates further documents associations between the hormone and body mass, growth rates, reproduction and survival (Addis, Gangloff, Palacios, Carr, & Bronikowski, 2017;Lewin, Swanson, Williams, & Holekamp, 2017;Lodjak, Mägi, Sild, & Mänd, 2017;Lodjak, Tilgar, & Mägi, 2016;Sparkman et al, 2010).…”

Food restriction delays breeding and affects insulin‐like growth factor‐1, oxidative damage and haematocrit value before egg‐laying in female canaries

“…An important circulating compound that is responsive to nutritional limitation and could exert an influence on reproduction is insulin‐like growth factor‐1 (IGF‐1). IGF‐1 is a pleiotropic peptide hormone regulating growth, body size, sexual maturation, reproductive investment and lifespan across a broad range of species (Baker et al 1993, Holzenberger et al 2003, Van Heemst et al 2010, Dantzer and Swanson 2012, Lodjak et al 2018, Lendvai et al 2021, Lodjak and Verhulst 2020). Fasting or low dietary protein intake was shown to decrease plasma IGF‐1 concentrations in various species including dairy cattle Bos taurus (Zulu et al 2002), Steller sea lions Eumetopias jubatus (du Dot et al 2009), domestic fowl Gallus gallus domesticus (Lauterio and Scanes 1987) and great tits Parus major (Lodjak et al 2014).…”

“…IGF‐1 plays an important role in the growth and maturation of reproductive tissues and gonadal steroidogenesis in fish (Weber and Sullivan 2000) and mammals (Daftary and Gore 2005, Pitetti et al 2013). Moreover, it is associated with life‐history variation in reptiles (Sparkman et al 2009, 2010), birds (Lodjak et al 2018) and mammals (Swanson and Dantzer 2014). However, very little is known about how IGF‐1 levels influence reproductive traits in birds, and the few studies so far have focused on poultry (Hocking et al 1994, McMurtry et al 1997, Onagbesan et al 1999, Kim et al 2004).…”

“…However, very little is known about how IGF‐1 levels influence reproductive traits in birds, and the few studies so far have focused on poultry (Hocking et al 1994, McMurtry et al 1997, Onagbesan et al 1999, Kim et al 2004). In free‐living passerines, there was one study that detected an association between plasma IGF‐1 levels and egg weight, and the direction of the association depended on the species' body weight (Lodjak et al 2018). Furthermore, it was reported that IGF‐1 could play a role in the development of sexually selected ornaments in a sexually dichromatic passerine species, the bearded reedling (Mahr et al 2020).…”