1 Lectures 9 & 10: Reproductive Biology and Behavior in fishBiology 450: Fish Week Lectures 9 & 10: Reproductive Biology and Behavior in fish Scott Heppell Department of Fisheries and Wildlife Oregon State University 042 Nash Hall ,

2 Fish Reproduction

3 The H-P-G axis Hypothalamus GnRH PIT GTH I/GTH II Testis OvarySex steroids

4 The HPG Feedback loops

5 Steroid biosynthesis

6 Hormonal control of oocyte maturation

7 Stages of maturation STAGE DESCRIPTION COMMENTS Stage 0 ImmatureNot capable of producing viable gametes Stage 1 Primary growth Resting or recently mature Stage 2 Secondary growth Vitellogenin independent, cortical alveoli present Stage 3 Early vitellogenesis Vitellogenin granules present, oocyte increasing in diameter Stage 4 Late vitellogenesis Strong presence of vitellogenin in oocyte, gametes approaching maximum pre-spawning diameter Stage 5 Mature/spawning/ Running ripe Hydrated oocytes, final maturation of gametes Stage 6 Spent High rates of atresia, gonad loosely organized

8 Stages of gonad maturation (female)Heppell and Sullivan FP&B 1999

9 The two-cell model

10 Vitellogenesis Hypothalamus GnRH PIT GTH I Ovary Vitellogenin LiverEstradiol Vitellogenin GTH I GnRH

11 Female final maturation

12 The female hormonal cycle

13 Water hardening

14 Hormonal control of sperm maturation

15 The male hormonal cycle

16 Male reproductive development

17 Quirks in reproductive assessment

18 Maternal effects Bobko and Berkeley 2004

19 Maternal effects Bobko and Berkeley 2004

20 Maternal effects Berkeley et al 2004

21 Maternal effects Berkeley et al 2004

22 Male mating strategiesGroup spawning –Sperm competitors Territoriality –Mate competitors Leks Nest guarding Sneaker, streakers, and satellite spawners

23 Nest guarding –Lingcod

24 Phase shifts in male reproductive tacticsImmature Mature ♀ ♂ ♀ ♂ ♂ Initial phase Immature ♂ Initial phase ♂ Terminal phase ♂

25 ♂ Initial phase Immature ♂ Initial phase ♂ Terminal phase ♂

26 Group spawning

27 Group spawning

28 Territoriality

29 Territoriality

30 Sex change

31 Types of hermaphroditismProtogyny- Female first Protandry –Male first Simultaneous –Can spawn as both at the same time

32 ♂/♀ ♂ ♀ ♂/♀ Sex change patterns ♀ ♂ U Immature Mature Immature Mature

33 Social control of sex change

34 Social control of sex changeWarner and Swearer (1991) Behaviors exhibited within minutes Color changes within a day Mature sperm within 8 days Semsar, Godwin, Grober, Bass Linked to Arginine Vasotosin production in the brain Not necessarily linked to gonad production of steroids Warner and Swearer 1991

35 Marlin explains to Nemo the sociological aspects of sexuality and parental role patterns within the context of the identity model for transgender and intersex inclusion

36 Sex ratio = 1:1 female:male

37 Sex ratio = 1.5:1 female:male

38 Sex ratio = 1:1 female:male

39 Sex ratio = 13:1 female:male

40 Department of Fisheries and Wildlife Oregon State UniversityBehavior, physiology, and life history comparisons in four species of grouper: What do they mean for grouper management? Scott A. Heppell Department of Fisheries and Wildlife Oregon State University

41 Marine fisheries ecology at multiple scales of biological organizationGrand unifying theory Molecule Cell Physiology Behavior Individual fitness Populations Species Communities Habitats Ecosystems Integration Management

42 Male reproductive tactics, disruption of mating strategies, and “The Challenge Hypothesis”Multiple strategies for reproductive success Primary/territorial males Aggressive High androgen levels Small testes Secondary males (Sneakers, streakers, and satellite males) Non-aggressive Low androgen levels Large testes Also the tactic of group spawners The challenge hypothesis (Wingfield 1984) Territoriality Aggression Mate competition Hormone positive feedback loops

43 Environmental input Behavioral interaction Sensory transductionTestis GTH Behavioral interaction Sensory transduction brain 11KT + Gene regulation Behavior Environmental input

44 A tale of four groupers

45 Male grouper reproductive life history analysisCollect gonad and plasma samples from males of three different species of grouper (Nassau, red hind, and gag, with an extant dataset for red grouper) Confirm stage of maturation w/histology Measure androgens (Testosterone, 11-ketotestosterone) Evaluate general patterns of androgens, sex ratio, gonadosomatic index, and spawning strategy to determine general life history patterns –identify implications for population level effects

46 Non-territorial, groupSpawning strategy Species Spawning strategy Agg. size E. striatus Non-territorial, group 1,000-10,000's E. guttatus Territorial, pair ’s E. morio 10's+ M. microlepis

47 Gonadosomatic index Species GSI Reference E. striatus 9.4Tucker et al (from figure) 10 Sadovy and Colin 1995 E. guttatus 0.66 Sadovy et al. 1994 E. morio 0.38 Alan Collins, unpublished 0.3 Johnson 1995 M. Microlepis 1.83 Hood and Schleider 1992 0.56 Collins et al. 1998

48 Sex ratio Species Sex ratio (M:F) Location Source E. striatus~2:1 to 1-1.4 Various Caribbean Sadovy and Colin 1995 E. guttatus 1:4 to 1:115 Puerto Rico Sadovy et al. 1994 1:4 to 1:8 Shapiro et al. 1993a E. morio 1:2 to 1:6 NE Gulf of Mexico Coleman et al. 1996 M. microlepis 1:5 to 1:76 Collins et al. 1998

49 Role of androgens in male reproductionTestosterone 11-ketotestosterone Sex differentiation and development Stimulates the pituitary to induce spermatogenesis Precursor to E2 and KT Territoriality Nest building Aggression Secondary sex characteristics Spermatogenesis and sperm maturation Tactic switching

50 Testosterone ANOVA p = 0.23 A A A A

51 11-ketotestosterone (Belize)ANOVA p <0.0001 Tukey HSD A B B B

52 11-ketotestosterone (Cayman)ANOVA p <0.0001 Tukey HSD A B B B

53 T:KT ratio (pooled samples)ANOVA p <0.001 LSD test A A A/B B

54 Environmental input Behavioral interaction Sensory transductionTestis GTH Behavioral interaction Sensory transduction brain 11KT + Gene regulation Behavior Environmental input

55 Decreased Individual Reproductive Success Population levelEnvironmental input Behavioral interaction Decreased Individual Reproductive Success Sensory transduction Gene regulation Behavior + brain Population level (Allee) effects? Down-regulated GTH Testis + 11KT

56 Conclusions Anatomy, behavior, and physiology, correlate with spawning strategy across four species of grouper This work presents a possible mechanism for depensation, at least in territorial species A wider variety of species should be investigated to see whether it holds true across the majority of grouper species For some species we should manage for sex ratio as well as overall spawning stock biomass Critical minimum population sizes may be necessary for patterned behaviors and effective spawning Assessing biological/resource issues across multiple scales of biological organization is important