In ovotemperature manipulation differentially influences limb musculoskeletal development in two lines of chick embryos selected for divergent growth rates

Abstract

SUMMARYSelective breeding has led to diverging phenotypic evolution in layer and broiler chickens through genomic and epigenetic modifications. Here we show that in ovo environmental manipulation differentially influences embryonic limb muscle phenotype in these two breeds. We demonstrate that raising incubation temperature from 37.5 to 38.5°C between embryonic days (ED) 4 and 7 increased motility and body mass in both layer and broiler embryos. In layers, this was accompanied by gastrocnemius muscle hypertrophy, increased fibre and nuclei numbers and a higher nuclei to fibre ratio (ED18), preceded by increased hindlimb Myf5 (ED5-8), Pax7 (ED5-10), BMP4 (ED6-9) and IGF-I (ED9-10, ED18) mRNAs. In broilers, the same temperature treatment led to reduced gastrocnemius cross-sectional area with fewer fibres and nuclei and an unchanged fibre to nuclei ratio (ED18). This was preceded by a delay in the peak of hindlimb Myf5 expression, increased Pax7 (ED5, ED7-10) and BMP4 (ED6-8) but reduced IGF-I (ED8-10) mRNAs. Rather than promoting myogenesis as in layer embryos, the temperature treatment promoted gastrocnemius intramuscular fat deposition in broilers (ED18) preceded by increased hindlimb PPAR mRNA (ED7-10). The treatment increased tibia/tarsus bone length as well as femur cross-sectional area in both breeds, but femur length and bone to cartilage ratio in the femur and tibia/tarsus were only increased in treated layers (ED18). We conclude that in ovo temperature manipulation differentially affected the molecular regulation of hindlimb myogenic, adipogenic and growth factor expression in broiler and layer embryos, leading to differential changes in muscle phenotype. The underlying interactive mechanisms between genes and the environment need further investigation.

The effect of temperature on apoptosis and adipogenesis on skeletal muscle satellite cells derived from different muscle types

“…2011; Al-Musawi et al. 2012). Such conversions of satellite cells from a myogenic to adipogenic lineage may also contribute to increased intramuscular fat depots that negatively impact treatment in individuals with diabetes mellitus (Hilton et al.…”

“…This finding is supported by Al-Musawi et al. (2012) who showed increased intramuscular fat deposition in the gastrocnemius muscle of 18-day-old chicks incubated for 3 days at one degree above normal in ovo incubation temperature. Taken together, the results from the present study support the conversion of myogenic satellite cells to an adipogenic pathway due to thermal manipulation.…”

Allen's Rule Revisited: Temperature Influences Bone Elongation During a Critical Period of Postnatal Development

“…Al-Musawi et al (2012) showed that higher egg incubation temperature alters expression of myogenic growth factors and increases muscle size in broiler chickens. While studies such as these reveal the importance of the genotypeenvironment interaction in early developmental programming, it is not as clear how phenotype is changed when exposures occur during later postnatal development.…”

Evidence in duck for supporting alteration of incubation temperature may have influence on methylation of genomic DNA

“…The incubation temperature design are listed in Figure 1. We divided the incubation stages into three phases, early embryonic stages (ED1–10), middle embryonic stages (ED10–20), later embryonic stages (ED20–27), which based on previous studies in birds (Collin et al., 2007; Hammond et al., 2007; Al-Musawi et al., 2012). Six ducklings were slaughtered by rapid bloodletting at ED10, 20 and 27.…”