Artificial selection reveals the role of transcriptional constraints in the maintenance of life history variation

Authors: PICK, JOEL - University Of Zurich; HATAKEYAMA, MASAOMI - University Of Zurich; Ihle, Kate; GASPARINI, JULIEN - The Sorbonne University; HAUSSEY, GLAUDY - The Sorbonne University; ISHISHITA, SATOSHI - Nagoya University; MATSUDA, YOICHI - Nagoya University; YOSHIMURA, TAKASHI - Nagoya University; KANOAKA, MASAHIRO - Nagoya University; SHIMIZU-INATSUGI, RIE - University Of Zurich; HIMIZU, KENTARO - University Of Zurich; TSCHIRREN, BARBARA - University Of Exeter

Submitted to: Evolution Letters
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/18/2020
Publication Date: 4/7/2020
Citation: Pick, J.L., Hatakeyama, M., Ihle, K.E., Gasparini, J., Haussey, G., Ishishita, S., Matsuda, Y., Yoshimura, T., Kanoaka, M.M., Shimizu-Inatsugi, R., Himizu, K.K., Tschirren, B. 2020. Artificial selection reveals the role of transcriptional constraints in the maintenance of life history variation. Evolution Letters. 4-3:200-211.
DOI: https://doi.org/10.1002/evl3.166

Interpretive Summary: Biologists have often observed that when resources are limited, an organism will need to make trade-offs between investing those resources in maintaining itself or producing offspring. Even though this type resource budgeting is wide-spread and an important part of our understanding of biology, surprisingly little is known about how these trade-offs are actually regulated at the molecular level. To begin to understand how this process works, we used quail that have been bred for large versus small eggs and measured differences in gene expression using whole transcriptome RNAseq. We found that even when the quail were given unlimited accesses to food, they still showed differences in gene expression suggesting a trade-off between reproduction and self-maintenance: birds that produced large eggs tended to have increased expression of genes associated with reproduction and decreased expression of genes associated with immunity and self-maintenance relative to those that produced small eggs. This may be important information for animals that are bred for production of meet and eggs.

Technical Abstract: The trade-off between reproduction and self-maintenance is a cornerstone of life-history theory, yet its proximate underpinnings are elusive. Here we used an artificial selection approach to create replicated lines of Japanese quail (Coturnix japonica) that differ genetically in their reproductive investment. Whole transcriptome sequencing revealed that females from lines selected for high reproductive output show a consistent upregulation of genes associated with reproduction but a simultaneous downregulation of immune genes. Concordant phenotypic differences in immune function (i.e. specific antibody response against KLH) were observed between the selection lines, even in males who do not provide parental care. Our findings demonstrate the key role of obligate transcriptional constraints in the maintenance of life-history variation. These constraints set fundamental limits to productivity and health in natural and domestic animal populations. A central tenet in life-history theory is that key functions, like reproduction and self-maintenance, trade-off against each other, preventing organisms from expressing perfect phenotypes. However, surprisingly little is known about the mechanisms underlying such fundamental trade-offs. Our experiments demonstrate that female birds artificially selected for high reproductive investment upregulate expression of genes associated with reproduction, but downregulate genes related to immune function. Immunosuppression at the phenotypic level was also observed in both sexes, despite males not contributing to parental care, and without of resource limitation, demonstrating its obligate nature. By linking evolutionary theory with mechanistic function, our study reveals that intrinsic constraints act to maintain diversity in life-histories, and set limits to productivity and health in natural and domesticated populations.