Abstract
Inbreeding often causes a decline in biological fitness, known as inbreeding depression. In genetics study, inbreeding coefficient f gives the proportion by which the heterozygosity of an individual is reduced by inbreeding. With the development of high-throughput sequencing, researchers were able to perform deep approaches to investigate which genes are affected by inbreeding and reveal some molecular underpinnings of inbreeding depression. As one commercially important species, Yesso scallop Patinopecten yessoensis confront the same dilemma of inbreeding depression. To examine how inbreeding affects gene expression, we compared the transcriptome of two experimentally selfing families with inbreeding coefficient f reached 0.5 as well as one natural population (f ≈ 0) of P. yessoensis. A total of 24 RNA-Seq libraries were constructed using scallop adductor muscle, and eventually 676.56 M (96.85%) HQ reads were acquired. Based on differential gene analysis, we were able to identify nine common differentially expressed genes (DEGs) across the top-ranked 30 DEGs in both selfing families in comparation with the natural population. Remarkable, through weighted gene co-expression network analysis (WGCNA), five common DEGs were found enriched in the most significant inbreeding related functional module M14 (FDR = 1.64E-156), including SREBP1, G3BP2, SBK1, KIAA1161, and AATs-Glupro. These five genes showed significantly higher expression in self-bred progeny. Suggested by the genetic functional analysis, up-regulated SREBP1, G3BP2, and KIAA1161 may suggest a perturbing lipid metabolism, a severe inframammary reaction or immune response, and a stress-responsive behavior. Besides, the significant higher SBK1 and AATs-Glupro may reflect the abnormal cellular physiological situation. Together, these genetic aberrant transcriptomic performances may contribute to inbreeding depression in P. yessoensis, deteriorating the stress tolerance and survival phenotype in self-bred progeny. Our results would lay a foundation for further comprehensive understanding of bivalve inbreeding depression, which may potentially benefit the genetic breeding for scallop aquaculture.
Similar content being viewed by others
Change history
23 January 2020
The original version of this article unfortunately contained a mistake in the authorgroup section. Author Zhenmin Bao’s given name was incorrectly spelled as “Zhemin Bao”.
23 January 2020
The original version of this article unfortunately contained a mistake in the authorgroup section. Author Zhenmin Bao���s given name was incorrectly spelled as ���Zhemin Bao���.
References
Aleng NA, Sung YY, MacRae TH, Abd Wahid ME (2015) Non-lethal heat shock of the Asian green mussel, Perna viridis, promotes Hsp70 synthesis, induces thermotolerance and protects against Vibrio infection. PLoS One 10:e0135603
Anders S, Pyl PT, Huber W (2015) HTSeq--a python framework to work with high-throughput sequencing data. Bioinformatics 31:166–169
Beissbarth T, Speed TP (2004) GOstat: find statistically overrepresented gene ontologies within a group of genes. Bioinformatics 20:1464–1465
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate - a practical and powerful approach to multiple testing. J R Stat Soc Ser B Stat Methodol 57:289–300
Burnell G, Allan G (eds) (2009) New technologies in aquaculture: improving production efficiency, quality and environmental management. Oxford, Woodhead Publishing
Caplins SA, Turbeville JM (2015) High rates of self-fertilization in a marine ribbon worm (Nemertea). Biol Bull 229:255–264
Charlesworth D, Willis JH (2009) The genetics of inbreeding depression. Nat Rev Genet 10:783–796
de Boer RA, Eens M, Fransen E, Muller W (2015) Hatching asynchrony aggravates inbreeding depression in a songbird (Serinus canaria): an inbreeding-environment interaction. Evolution 69:1063–1068
Dheilly NM, Lelong C, Huvet A, Favrel P (2011) Development of a Pacific oyster (Crassostrea gigas) 31,918-feature microarray: identification of reference genes and tissue-enriched expression patterns. BMC Genomics 12:468
Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR (2013) STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 29:15–21
Enders LS, Nunney L (2012) Seasonal stress drives predictable changes in inbreeding depression in field-tested captive populations of Drosophila melanogaster. Proc R Soc B Biol Sci 279:3756–3764
Fearnside JF, Dumas ME, Rothwell AR, Wilder SP, Cloarec O, Toye A, Blancher C, Holmes E, Tatoud R, Barton RH, Scott J, Nicholson JK, Gauguier D (2008) Phylometabonomic patterns of adaptation to high fat diet feeding in inbred mice. PLoS One 3:e1668
Fellous A, Labed-Veydert T, Locrel M, Voisin AS, Earley RL, Silvestre F (2018) DNA methylation in adults and during development of the self-fertilizing mangrove rivulus, Kryptolebias marmoratus. Ecol Evol 8:6016–6033
Fox CW, Reed DH (2011) Inbreeding depression increases with environmental stress: an experimental study and meta-analysis. Evolution 65:246–258
Frankham R, Ralls K (1998) Conservation biology - inbreeding leads to extinction. Nature 392:441–442
Fu X, Sun Y, Wang J, Xing Q, Zou J, Li R, Wang Z, Wang S, Hu X, Zhang L, Bao Z (2014) Sequencing-based gene network analysis provides a core set of gene resource for understanding thermal adaptation in Zhikong scallop Chlamys farreri. Mol Ecol Resour 14:184–198
Goto K, Oda H, Kondo H, Igaki M, Suzuki A, Tsuchiya S, Murase T, Hase T, Fujiya H, Matsumoto I, Naito H, Sugiura T, Ohira Y, Yoshioka T (2011) Responses of muscle mass, strength and gene transcripts to long-term heat stress in healthy human subjects. Eur J Appl Physiol 111:17–27
Hedgecock D, Lin JZ, DeCola S, Haudenschild CD, Meyer E, Manahan DT, Bowen B (2007) Transcriptomic analysis of growth heterosis in larval Pacific oysters (Crassostrea gigas). Proc Natl Acad Sci U S A 104:2313–2318
Hedrick PW, Garcia-Dorado A (2016) Understanding inbreeding depression, purging, and genetic rescue. Trends Ecol Evol 31:940–952
Hoffman JI, Simpson F, David P, Rijks JM, Kuiken T, Thorne MAS, Lacy RC, Dasmahapatra KK (2014) High-throughput sequencing reveals inbreeding depression in a natural population. Proc Natl Acad Sci U S A 111:3775–3780
Hoffmann AA, Sgro CM, Kristensen TN (2017) Revisiting adaptive potential, population size, and conservation. Trends Ecol Evol 32:506–517
Hong HQ, Lu J, Fang XL, Zhang YH, Cai Y, Yuan J, Liu PQ, Ye JT (2018) G3BP2 is involved in isoproterenol-induced cardiac hypertrophy through activating the NF-kappaB signaling pathway. Acta Pharmacol Sin 39:184–194
Janicke T, Vellnow N, Lamy T, Chapuis E, David P (2014) Inbreeding depression of mating behavior and its reproductive consequences in a freshwater snail. Behav Ecol 25:288–299
Kardos M, Taylor HR, Ellegren H, Luikart G, Allendorf FW (2016) Genomics advances the study of inbreeding depression in the wild. Evol Appl 9:1205–1218
Lamas O, Moreno-Aliaga MJ, Martinez JA, Marti A (2003) NF-kappa B-binding activity in an animal diet-induced overweightness model and the impact of subsequent energy restriction. Biochem Biophys Res Commun 311:533–539
Lang RP, Bayne CJ, Camara MD, Cunningham C, Jenny MJ, Langdon CJ (2009) Transcriptome profiling of selectively bred Pacific oyster Crassostrea gigas families that differ in tolerance of heat shock. Mar Biotechnol 11:650–668
Langfelder P, Horvath S (2008) WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 9:559
Lee HC, Chang DE, Yeom M, Kim GH, Choi KD, Shim I, Lee HJ, Hahm DH (2005) Gene expression profiling in hypothalamus of immobilization-stressed mouse using cDNA microarray. Mol Brain Res 135:293–300
Li Q, Xu K, Yu R (2007) Genetic variation in Chinese hatchery populations of the Japanese scallop (Patinopecten yessoensis) inferred from microsatellite data. Aquaculture 269:211–219
Li RJ, Zhang R, Zhang L, Zou JJ, Xing Q, Dou HQ et al (2015) Characterizations and expression analyses of NF-kappaB and Rel genes in the yesso scallop (Patinopecten yessoensis) suggest specific response patterns against gram-negative infection in bivalves. Fish Shellfish Immunol 44:611–621
Li SL, Li ZQ, Chen NS, Jin PF, Zhang JC (2019) Dietary lipid and carbohydrate interactions: implications on growth performance, feed utilization and non-specific immunity in hybrid grouper (Epinephelus fuscoguttatus female x E-lanceolatus male). Aquaculture 498:568–577
Liao W, Reed DH (2009) Inbreeding-environment interactions increase extinction risk. Anim Conserv 12:54–61
Liu Y, Xu C, Tang XB, Pei SR, Jin D, Guo MH et al (2018) Genomic methylation and transcriptomic profiling provides insights into heading depression in inbred Brassica rapa L. ssp pekinensis. Gene 665:119–126
Menzel M, Sletvold N, Agren J, Hansson B (2015) Inbreeding affects gene expression differently in two self-incompatible Arabidopsis lyrata populations with similar levels of inbreeding depression. Mol Biol Evol 32:2036–2047
Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35:W182–W185
Murphy S, Zweyer M, Henry M, Meleady P, Mundegar RR, Swandulla D, Ohlendieck K (2018) Subproteomic profiling of sarcolemma from dystrophic mdx-4cv skeletal muscle. Data Brief 17:980–993
Nascimento-Sales M, Fredo-da-Costa I, Borges Mendes ACB, Melo S, Ravache TT, Gomez TGB, Gaisler-Silva F, Ribeiro MO, Santos AR Jr, Carneiro-Ramos MS, Christoffolete MA (2017) Is the FVB/N mouse strain truly resistant to diet-induced obesity? Physiol Rep 5:e13271
Ozsolak F, Milos PM (2011) RNA sequencing: advances, challenges and opportunities. Nat Rev Genet 12:87–98
Pérez HM, Janssoone X, Nadeau M, Guderley H (2008) Force production during escape responses by Placopecten magellanicus is a sensitive indicator of handling stress: comparison with adductor muscle adenylate energy charge and phosphoarginine levels. Aquaculture 282:142–146
Phillippi AL, Yund PO (2017) Self-fertilization and inbreeding depression in three ascidian species that differ in genetic dispersal potential. Mar Biol 164:179
Plough LV (2012) Environmental stress increases selection against and dominance of deleterious mutations in inbred families of the Pacific oyster Crassostrea gigas. Mol Ecol 21:3974–3987
Plough LV, Hedgecock D (2011) Quantitative trait locus analysis of stage-specific inbreeding depression in the Pacific oyster Crassostrea gigas. Genetics 189:1473–1486
Ponomarev I, Wang S, Zhang LL, Harris RA, Mayfield RD (2012) Gene coexpression networks in human brain identify epigenetic modifications in alcohol dependence. J Neurosci 32:1884–1897
Reed DH, Fox CW, Enders LS, Kristensen TN (2012) Inbreeding-stress interactions: evolutionary and conservation consequences. Year Evol Biol 1256:33–48
Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140
Rosche C, Hensen I, Lachmuth S (2018) Local pre-adaptation to disturbance and inbreeding-environment interactions affect colonisation abilities of diploid and tetraploid Centaurea stoebe. Plant Biol 20:75–84
Schou MF, Loeschcke V, Kristensen TN (2015) Inbreeding depression across a nutritional stress continuum. Heredity 115:56–62
Schou MF, Bechsgaard J, Munoz J, Kristensen TN (2018) Genome-wide regulatory deterioration impedes adaptive responses to stress in inbred populations of Drosophila melanogaster. Evolution 72:1614–1628
Schrieber K, Lachmuth S (2017) The genetic paradox of invasions revisited: the potential role of inbreeding x environment interactions in invasion success. Biol Rev 92:939–952
Venney CJ, Johansson ML, Heath DD (2016) Inbreeding effects on gene-specific DNA methylation among tissues of Chinook salmon. Mol Ecol 25:4521–4533
Wang PZ, Guo JH, Wang F, Shi TP, Ma DL (2011) Human SBK1 is dysregulated in multiple cancers and promotes survival of ovary cancer SK-OV-3 cells. Mol Biol Rep 38:3551–3559
Wang W, Hui JHL, Chan TF, Chu KH (2014) De novo transcriptome sequencing of the snail Echinolittorina malaccana: identification of genes responsive to thermal stress and development of genetic markers for population studies. Mar Biotechnol 16:547–559
Wang S, Zhang JB, Jiao WQ, Li J, Xun XG, Sun Y et al (2017) Scallop genome provides insights into evolution of bilaterian karyotype and development. Nat Ecol Evol 1:120
Wei G, Tao Y, Liu GZ, Chen C, Luo RY, Xia HA et al (2009) A transcriptomic analysis of superhybrid rice LYP9 and its parents. Proc Natl Acad Sci U S A 106:7695–7701
Yadetie F, Oveland E, Doskeland A, Berven F, Goksoyr A, Karlsen OA (2017) Quantitative proteomics analysis reveals perturbation of lipid metabolic pathways in the liver of Atlantic cod (Gadus morhua) treated with PCB 153. Aquat Toxicol 185:19–28
Yan LL, Su JQ, Wang ZP, Zhang YH, Yan XW, Yu RH (2018) Growth performance and biochemical composition of the oysters Crassostrea sikamea, Crassostrea angulata and their hybrids in southern China. Aquac Res 49:1020–1028
Yang H, Wang XC, Wei YX, Deng Z, Liu H, Chen JS et al (2018) Transcriptomic analyses reveal molecular mechanisms underlying growth heterosis and weakness of rubber tree seedlings. BMC Plant Biol 18:10
Zajitschek SRK, Brooks RC (2010) Inbreeding depression in male traits and preference for outbred males in Poecilia reticulata. Behav Ecol 21:884–891
Zhang B, Horvath S (2005) A general framework for weighted gene co-expression network analysis. Stat Appl Genet Mol Biol 4. https://doi.org/10.2202/1544-6115.1128
Zhang LL, Hou R, Su HL, Hu XL, Wang S, Bao ZM (2012) Network analysis of oyster transcriptome revealed a cascade of cellular responses during recovery after heat shock. PLoS One 7:e35484
Zhao C, Sun P, Wei J, Zhang LS, Zhang WJ, Song J et al (2016) Larval size and metamorphosis are significantly reduced in second generation of inbred sea urchins Strongylocentrotus intermedius. Aquaculture 452:402–406
Zheng HP, Li L, Zhang GF (2012) Inbreeding depression for fitness-related traits and purging the genetic load in the hermaphroditic bay scallop Argopecten irradians irradians (Mollusca: Bivalvia). Aquaculture 366:27–33
Zhou T, Yuan ZH, Tan SX, Jin YL, Yang YJ, Shi HT et al (2018) A review of molecular responses of catfish to bacterial diseases and abiotic stresses. Front Physiol 9:1113
Funding
This work was supported by the National Natural Science Foundation of China [grant no. (31802295)], and Youth Talent Program Supported by Laboratory for Marine Fisheries Science and Food Production Processes, Pilot National Laboratory for Marine Science and Technology (Qingdao) [grant no. (2018-MFS-T06)].
Author information
Authors and Affiliations
Contributions
SL, XH, and ZB conceived and designed the experiments; QF and LZ performed the experiments; YL analyzed the data; JL, ZY, HL, and ZG contributed reagents/materials/analysis tools; SL and LZ wrote the paper.
Corresponding author
Ethics declarations
Data Availability
The transcriptomic data used in the present research can be achieved on SRA database (PRJNA515834).
Conflict of Interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic Supplementary Material
ESM 1
(XLSX 471 kb)
Rights and permissions
About this article
Cite this article
Zhao, L., Li, Y., Lou, J. et al. Transcriptomic Profiling Provides Insights into Inbreeding Depression in Yesso Scallop Patinopecten yessoensis. Mar Biotechnol 21, 623–633 (2019). https://doi.org/10.1007/s10126-019-09907-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10126-019-09907-9