fishes Review Oogenesis and Egg Quality in Finfish: Yolk Formation and Other Factors Influencing Female Fertility Benjamin J. Reading 1,2,*, Linnea K. Andersen 1, Yong-Woon Ryu 3, Yuji Mushirobira 4, Takashi Todo 4 and Naoshi Hiramatsu 4 1 Department of Applied Ecology, North Carolina State University, Raleigh, NC 27695, USA; [email protected] 2 Pamlico Aquaculture Field Laboratory, North Carolina State University, Aurora, NC 27806, USA 3 National Institute of Fisheries Science, Gijang, Busan 46083, Korea; [email protected] 4 Faculty of Fisheries Sciences, Hokkaido University, Minato, Hakodate, Hokkaido 041-8611, Japan; [email protected] (Y.M.); todo@fish.hokudai.ac.jp (T.T.); naoshi@fish.hokudai.ac.jp (N.H.) * Correspondence: [email protected]; Tel.: +1-919-515-3830 Received: 28 August 2018; Accepted: 16 November 2018; Published: 21 November 2018 Abstract: Egg quality in fishes has been a topic of research in aquaculture and fisheries for decades as it represents an important life history trait and is critical for captive propagation and successful recruitment. A major factor influencing egg quality is proper yolk formation, as most fishes are oviparous and the developing offspring are entirely dependent on stored egg yolk for nutritional sustenance. These maternally derived nutrients consist of proteins, carbohydrates, lipids, vitamins, minerals, and ions that are transported from the liver to the ovary by lipoprotein particles including vitellogenins. The yolk composition may be influenced by broodstock diet, husbandry, and other intrinsic and extrinsic conditions. In addition, a number of other maternal factors that may influence egg quality also are stored in eggs, such as gene transcripts, that direct early embryonic development. Dysfunctional regulation of gene or protein expression may lead to poor quality eggs and failure to thrive within hours of fertilization. These gene transcripts may provide important markers as their expression levels may be used to screen broodstock for potential spawning success. In addition to such intrinsic factors, stress may lead to ovarian atresia or reproductive failure and can impact fish behavior, fecundity, and ovulation rate. Finally, postovulatory aging may occur when eggs become overripe and the fish fails to spawn in a timely fashion, leading to low fertility, often encountered during manual strip spawning of fish. Keywords: egg quality; vitellogenin; aquaculture; fish; fertility; oogenesis; yolk; reproduction 1. Introduction Reproductive fitness is a critical component to the success of wild and domestic animals and egg quality of fishes has been a topic of research for decades in regards to aquaculture and fisheries. The study of egg quality is complex, as “quality” can be defined in different contexts and also is influenced by a variety of factors both intrinsic and extrinsic to the animal. The term egg quality has generally been defined as the ability of developmentally competent eggs to produce viable embryos once fertilized by a sperm [1–4]. Although simple in context, this is a much more complicated concept to understand in practice. The intent of this review is to provide an overview of oogenesis, yolk formation, ovarian maturation, and ovulation with special attention paid to our understanding of how these processes may become dysfunctional leading to poor egg quality. Identifying what makes a “poor quality” egg first requires an understanding of how a “good quality” egg is formed. Fishes 2018, 3, 45; doi:10.3390/fishes3040045 www.mdpi.com/journal/fishes Fishes 2018, 3, 45 2 of 28 Fishes 2018, 3, x FOR PEER REVIEW 2 of 27 2.2. Ovarian Ovarian Growth Growth and and Yolk Yolk Formation Formation GrowthGrowth of of ovarian ovarian follicles follicles can can be be broadly broadly divided divided into into previtellogenic previtellogenic and and vitellogenic vitellogenic growth growth stages,stages, during during which which the the major major lipid lipid and and protein protein nutrients nutrients required required for for embryonic embryonic and and larval larval developmentdevelopment are are stored stored within within the the oocyte oocyte (this (this review review will will generally generally follow follow those those processes processes outlined outlined inin Figure Figure 11).). Previtellogenic oocytes begin to accumulate neutral lipids, which are stored as lipidlipid dropletsdroplets in in the the ooplasm, ooplasm, and and also also accumulate accumulate matern maternalal gene gene transcripts, transcripts, wh whichich function function to to direct direct earlyearly embryonic embryonic development development shortly shortly following following fert fertilization.ilization. Vitellogenic Vitellogenic stage stage oocytes oocytes accumulate accumulate phospholipid-richphospholipid-rich lipoproteins,lipoproteins, which which are storedare stored as yolk as inclusions yolk inclusions in the ooplasm. in the When ooplasm. vitellogenesis When vitellogenesisends, the ovary ends, is filled the with ovary fully is yolked filled oocytes with fully that subsequentlyyolked oocytes undergo that maturationsubsequently and ovulation.undergo maturationThe entire and period ovulation. encompassed The entire by period previtellogenic encompassed and by vitellogenic previtellogenic growth and is vitellogenic typically a growth critical istimeframe typically a for critical captive timeframe broodstock for managementcaptive broodstock as appropriate management conditioning as appropriate and diet conditioning are required and for dietthe animalsare required to produce for the goodanimal qualitys to produce eggs. good quality eggs. MGT Meiosis Em bryonic gene expression O ocyte grow th Ovary maturation E a rly & la te e m b ry o g e n e s is fo llic u lo - m a tu ra tio n a l ovulation hatch genesis com petence deposition of fe rtiliz a tio n em bryo y o lk & o th e r larval maternal genom ic and cytoplasmic nutrition & developm ent nutrition & factors m a tu ra tio n developm ent Vitellogenesis Yolk processing Em bryo survival Larval survival Lipidation G erm inal vesicle breakdow n Physical deform ities M aternal gene transcripts Postovulatory aging O varian atresia F e rtility Proper Broodstock Proper Induction of Proper Hatchery Conditions H usbandry and Diet O vulation and Spaw ning and Juvenile Rearing FigureFigure 1. ModelModeldepicting depicting the the summary summary of processes of processe ands events and duringevents oocyteduring growth, oocyte ovary growth, maturation, ovary maturation,and early and and late early embryogenesis and late embryogenesis in fishes. Vertical in greyfishes. arrows Vertical indicate grey critical arrows physiological indicate critical events, physiologicalhorizontal black events, arrows horizontal indicate bl importantack arrows processes, indicate important and open arrowsprocesses, indicate and open potential arrows problems indicate or potentialevaluations problems of egg quality. or evaluations These topics of egg are quality. detailed Th inese corresponding topics are detailed sections ofin thiscorresponding review and thesections figure ofhas this been review compiled and from the several figure studies has includingbeen comp thoseiled on: from folliculogenesis, several studies vitellogenesis, including lipidation, those on: and folliculogenesis,yolk processing [vitellogenesis,5–41]; maternal lip geneidation, transcripts and yolk [2–4 ,processing42–51]; maturational [5–41]; maternal competence, gene germinaltranscripts vesicle [2– 4,42–51];breakdown, maturational cytoplasmic competence, maturation, andgerminal ovulation vesi [15cle,25 breakdown,,26,30,31,35,52 cytopl–57]; ovarianasmic maturation, atresia (including and ovulationbroodstock [15,25,26,30,31,35,52–57]; stress) [48,52,58–70]; postovulatory ovarian atre agingsia [ 48(including,71–85]; and broodstock methods of stress) evaluating [52,48,58–70]; egg quality postovulatoryincluding fertility, aging embryo [48,71–85]; survival, and larval methods survival, of andevalua incidenceting egg of physicalquality deformitiesincluding fertility, [3,42,43, 45embryo–51,86]. survival,Proper broodstock larval survival, husbandry and incidence and diet, of physic conditioningal deformities for spawning, [3,42,43,45–51,86]. ovulation, Proper fertilization, broodstock and husbandryhatchery conditions and diet, conditioning are required for to spawning, produce high ovul qualityation, fertilization, eggs, see also: and [ 1hatchery,3,15,25,52 conditions,53,58,87– 131are]. requiredMGT = translation to produce of maternalhigh quality gene eggs, transcripts. see also: [1,3,52,53,15,25,58,87–131]. MGT = translation of maternal gene transcripts. In many teleosts, large amounts of neutral lipids are accumulated in oocyte lipid droplets during early oocyte growth in a process termed ‘oocyte lipidation’. The occurrence of lipid droplets is generally firstIn observed many teleosts, at the large previtellogenic amounts of oocyteneutral growthlipids are stage, accumulated and ongoing in oocyte accumulation lipid droplets continues during earlyas development oocyte growth proceeds in a process through termed vitellogenesis ‘oocyte li [132pidation’.]. Recent The studies occurrence in Japanese of lipid eel droplets (Anguilla is generallyjaponica)[ 5first], shortfinned observed eelat (theAnguilla previtellogenic australis)[ 6oocyte], cutthroat growth trout st (age,Oncorhynchus and ongoing clarkii accumulation), [7], medaka, continues as development proceeds through vitellogenesis [132]. Recent studies in Japanese