Proteomic insight into human directed selection of the domesticated chicken Gallus gallus.

PLOS ONE RESEARCH ARTICLE Proteomic insight into human directed selection of the domesticated chicken Gallus gallus. Carl J. Schmidt ID1*, Dong Kyun Kim ID2, G Ken Pendarvis3, Behnam Abasht ID1, Fiona M. McCarthy ID3* a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 1 Department of Animal and Food Sciences, University of Delaware, Newark, Delaware, United States of America, 2 Center for Innovation in Brain Sciences, University of Arizona, Tucson, Arizona, United States of America, 3 School of Animal and Comparative Biomedical Sciences, University of Arizona, Tucson, Arizona, United States of America * (FMM); (CJS) Abstract OPEN ACCESS Citation: Schmidt CJ, Kim DK, Pendarvis GK, Abasht B, McCarthy FM (2023) Proteomic insight into human directed selection of the domesticated chicken Gallus gallus.. PLoS ONE 18(8): e0289648. https://doi.org/10.1371/journal.pone.0289648 Editor: Lamiaa Mostafa Radwan, Ain Shams University Faculty of Agriculture, EGYPT Received: April 19, 2023 Accepted: July 21, 2023 Published: August 7, 2023 Copyright: © 2023 Schmidt et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: Transcript data discussed in this publication have been deposited in NCBI’s Gene Expression Omnibus (GEO) with accession number GSE65217 (https://www.ncbi. nlm.nih.gov/geo/query/acc.cgi?acc=GSE65217). Proteomics data is available from ProteomeXchange with accession number PXD005288 (https://proteomecentral. proteomexchange.org/cgi/GetDataset?ID= PXD005288). Funding: CJS was supported by the Agriculture and Food Research Institute competitive grant Chicken domestication began at least 3,500 years ago for purposes of divination, cockfighting, and food. Prior to industrial scale chicken production, domestication selected larger birds with increased egg production. In the mid-20th century companies began intensive selection with the broiler (meat) industry focusing on improved feed conversion, rapid growth, and breast muscle yield. Here we present proteomic analysis comparing the modern broiler line, Ross 708, with the UIUC legacy line which is not selected for growth traits. Breast muscle proteome analysis identifies cellular processes that have responded to human directed artificial selection. Mass spectrometry was used to identify protein level differences in the breast muscle of 6-day old chicks from Modern and Legacy lines. Our results indicate elevated levels of stress proteins, ribosomal proteins and proteins that participate in the innate immune pathway in the Modern chickens. Furthermore, the comparative analyses indicated expression differences for proteins involved in multiple biochemical pathways. In particular, the Modern line had elevated levels of proteins affecting the pentose phosphate pathway, TCA cycle and fatty acid oxidation while proteins involved in the first phase of glycolysis were reduced compared to the Legacy line. These analyses provide hypotheses linking the morphometric changes driven by human directed selection to biochemical pathways. These results also have implications for the poultry industry, specifically Wooden Breast disease which is linked to rapid breast muscle growth. Introduction The chicken has played an important role in human culture and nutrition since its domestication [1,2]. The majority of the modern chicken’s genome was derived from the red junglefowl with documented introgression of alleles from the grey, Ceylon, and green junglefowl [3]. Early domestication likely led to larger birds that matured quicker and increased egg production in comparison with their wild progenitors [4,5]. The advent of modern agriculture in the PLOS ONE | https://doi.org/10.1371/journal.pone.0289648 August 7, 2023 1 / 17 PLOS ONE (2011-67003-30228) from the United States Department of Agriculture National Institute of Food and Agriculture The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. Domestication of the modern broiler chicken early 20th century led to intensive genetic selection for either meat (broiler) or egg (layer) production traits in the chicken. Initial efforts selecting for increased broiler mass led to adipose tissue accumulation, probably because the selection did not channel the increased level of nutrients to a particular tissue [6]. Ultimately, improving broiler production traits led to selection for a combination of larger breast muscle mass, improved feed efficiency and rapid growth. Comparative studies describing differences between selected and unselected (legacy) lines provide insight into the impact of artificial selection of species. Several studies have characterized the differences between modern broilers and legacy lines that have not been subjected to production level human directed selection [7–13]. In our work [14–16] we compared the modern Ross 708 broiler line and the legacy University of Illinois, Urbana Campus (UIUC) lines (Fig 1) [17,18]. In the legacy line the breast muscle comprises approximately 9% of the body mass, while in the modern broiler this tissue constitutes up to 22% of the body mass [14]. Evolving in the tropics, the red junglefowl had little need for long distance flying. The wild chicken is an episodic flier, only needing the ability to fly up into a tree to escape predators and to roost. Like the legacy line, the breast muscle of the red junglefowl constitutes approximately 9% of its body mass [19]. For comparison, the breast muscle of birds capable of more sustained flight averages 17% while that of hummingbirds varies between 25–30% [20]. Fig 1. Results of artificial selection for increased feed efficiency and breast muscle yield. Comparison of 35-day old male UIUC legacy chicken (left) with a 35-day old male Ross 708 chicken (right). The UIUC bird is typical in size and shape for a chicken from the 1950s while the Ross 708 bird is from a modern commercial flock grown for human consumption. https://doi.org/10.1371/journal.pone.0289648.g001 PLOS ONE | https://doi.org/10.1371/journal.pone.0289648 August 7, 2023 2 / 17 PLOS ONE Domestication of the modern broiler chicken The increase in the modern broiler’s breast muscle mass, which almost reaches the hummingbird level, came at the expense of other tissues. For example, the normalized masses of the heart, spleen and brain are larger in legacy lines compared with modern broilers [13,14,21]. In modern broilers, this likely is responsible for increased incidence of cardiomyopathy [22,23] and immune deficiencies [10]. The reduced brain mass in broilers could contribute to the behavioral differences seen in modern broilers compared with other lines. The (...truncated)