Simultaneous courtship and parenting in males and sex role reversal in females of the haremic bluebanded goby, Lythrypnus dalli

in Behaviour
Restricted Access
Get Access to Full Text
Rent on DeepDyve

Have an Access Token?

Enter your access token to activate and access content online.

Please login and go to your personal user account to enter your access token.


Have Institutional Access?

Access content through your institution. Any other coaching guidance?


While males typically compete for females, species with female biased sex ratios and/or large male investment in offspring care often exhibit reversed sex roles. Here we investigated, in a haremic fish species, the bluebanded goby, Lythrypnus dalli, the impact of male and female courtship behaviour on male reproductive success, measured as the total number of eggs in the nest and total number of developed eggs. Reproductive success was not associated with rates of male behaviour, such as parenting, approaching and courtship, but was associated with rates of female courtship. Consistent with predictions for a role-reversed reproductive strategy, only males demonstrated nest care and females exhibited high rates of courtship and intrasexual competition, such that alpha females interrupted courtship solicitations by beta females. Overall, these data are consistent with sex role reversal in L. dalli and show that the expression of male courtship behaviour does not interfere with paternal care.

Simultaneous courtship and parenting in males and sex role reversal in females of the haremic bluebanded goby, Lythrypnus dalli

in Behaviour



AlcockJ. (2001). Animal behavior: an evolutionary approach. — Sinauer AssociatesSunderland, MA.

AngT.Z.ManicaA. (2010). Benefits and costs of dominance in the angelfish Centropyge bicolor. — Ethology 116: 855-865.

Balshine-EarnS.NeatF.C.ReidH.TaborskyM. (1998). Paying to stay or paying to breed? Field evidence for direct benefits of helping behavior in a cooperatively breeding fish. — Behav. Ecol. 9: 432-438.

BarrettJ.AbbottD.GeorgeL. (1993). Sensory cues and the suppression of reproduction in subordinate female marmoset monkeys, Callithrix jacchus. — J. Reprod. Fertil. 97: 301-310.

BeachF.A. (1976). Sexual attractivity, proceptivity, and receptivity in female mammals. — Horm. Behav. 7: 105-138.

BehrentsK.C. (1987). The influence of shelter availability on recruitment and early juvenile survivorship of Lythrypnus dalli Gilbert (Pisces: Gobiidae). — J. Exp. Mar. Biol. Ecol. 107: 47-59.

BlackM.P.MooreB.CanarioA.V.M.FordD.ReavisR.H.GroberM.S. (2005). Reproduction in context: field testing a laboratory model of socially controlled sex change in Lythrypnus dalli (Gilbert). — J. Exp. Mar. Biol. Ecol. 318: 127-143.

BushS.L.BellD.J. (1997). Courtship and female competition in the Majorcan midwife toad, Alytes muletensis. — Ethology 103: 292-303.

DarwinC. (1871). The descent of man and selection in relation to sex. — D. AppletonNew York, NY.

EllisL. (1995). Dominance and reproductive success among nonhuman animals: a cross-species comparison. — Ethol. Sociobiol. 16: 257-333.

FitzpatrickJ.DesjardinsJ.MilliganN.StiverK.MontgomerieR.BalshineS. (2008). Female-mediated causes and consequences of status change in a social fish. — Proc. Roy. Soc. Lond. B: Biol. Sci. 275: 929-936.

FlamariqueI.N.BergstromC.ChengC.L.ReimchenT.E. (2013). Role of the iridescent eye in stickleback female mate choice. — J. Exp. Biol. 216: 2806-2812.

ForsgrenE. (2007). Female sand gobies prefer good fathers over dominant males. — Proc. Roy. Soc. Lond. B: Biol. Sci. 264: 1283-1286.

ForsgrenE.KarlssonA.KvarnemoC. (1996). Female sand gobies gain direct benefits by choosing males with eggs in their nests. — Behav. Ecol. Sociobiol. 39: 91-96.

GriggioM.MingozziT.BortolinF.PilastroA. (2008). Trade-off between sexual activities and parental care: an experimental test using handicapped mates. — Ethol. Ecol. Evol. 20: 155-164.

GrossM.R.SargentR.C. (1985). The evolution of male and female parental care in fishes. — Am. Zool. 25: 807-822.

HegD. (2008). Reproductive suppression in female cooperatively breeding cichlids. — Biol. Lett. 4: 606-609.

KarinoK. (1995). Effective timing of male courtship displays for female mate choice in a territorial damselfish Stegastes nigricans. — Jpn. J. Ichthyol. 42: 173-180.

KarinoL.AraiR. (2006). Effect of clutch size on male egg-fanning behavior and hatching success in the goby, Eviota prasina (Klunzinger). — J. Exp. Mar. Biol. Ecol. 334: 43-50. AraújoA.M. (2010). Courtship behavior of Heliconius erato phyllis (Lepidoptera, Nymphalidae) towards virgin and mated females: conflict between attraction and repulsion signals?J. Ethol. 28: 409-420.

KnappR.A.KovachJ.T. (1991). Courtship as an honest indicator of male parental quality in the bicolor damselfish, Stegastes partitus. — Behav. Ecol. 2: 295-300.

KokkoH.JennionsM.D. (2008). Parental investment, sexual selection and sex ratios. — J. Evol. Biol. 21: 919-948.

LindströmK. (1992). Female spawning patterns and male mating success in the sand goby Pomatoschistus minutus. — Mar. Biol. 113: 475-480.

LorenziV. (2009). The behavioral neuroendocrinology of fish sex change: role of steroids and monoamines. — PhD thesis Georgia State University Atlanta GA.

MacLarenR.D.RowlandW.J. (2006). Differences in female preference for male body size in Poecilia latipinna using simultaneous versus sequential stimulus presentation designs. — Behaviour 143: 273-292.

MarconattoA.BisazzaA. (1986). Males whose nests contain eggs are preferred by female Cottus gobio L. (Pisces, Cottidae). — Anim. Behav. 34: 1580-1582.

MarconattoA.RasottoM.B.MazzoldiC. (1996). On the mechanism of sperm release in three gobiid fishes (Teleostei: Gobiidae). — Env. Biol. Fish. 46: 327-327.

MillerD.J.LeaR.N. (1972). Guide to the coastal marine fishes of California. — In: California Department of Fish and Game Fish Bulletin 157. California Department of Fish and Game Sacramento CA.

OkanoyaK. (2004). Song syntax in Bengalese finches: proximate and ultimate analyses. — In: Advances in the study of behavior ( SlaterP.J.B.RosenblattJ.S.SnowdownC.T.RoperT.J.BrockmannH.J.NaguibM. eds). Elsevier Academic PressSan Diego, CA p.  304-309.

PradhanD.S.ConnorK.R.PritchettE.M.GroberM.S. (2014a). Contextual modulation of androgen effects on agonistic interactions. — Horm. Behav. 65: 47-56.

PradhanD.S.Solomon-LaneT.K.WillisM.C.GroberM.S. (2014b). A mechanism for rapid neurosteroidal regulation of parenting behaviour. — Proc. Roy. Soc. Lond. B: Biol. Sci. 281: 20140239.

ReavisR.H.GroberM.S. (1999). An integrative approach to sex change: social, behavioural and neurochemical changes in Lythrypnus dalli (Pisces). — Acta Ethol. 2: 51-60.

RodgersE.W.EarleyR.L.GroberM.S. (2007). Social status determines sexual phenotype in the bi-directional sex changing bluebanded goby Lythrypnus dalli. — J. Fish Biol. 70: 1660-1668.

RosenblattJ.S. (2003). Outline of the evolution of behavioral and nonbehavioral patterns of parental care among the vertebrates: critical characteristics of mammalian and avian parental behavior. — Scand. J. Psychol. 44: 265-271.

RowlandW.J.GrindleN.MacLarenR.D.GranquistR. (2002). Male preference for a subtle posture cue that signals spawning readiness in female sticklebacks. — Anim. Behav. 63: 743-748.

RutowskiR.L. (1984). Sexual selection and the evolution of butterfly mating behaviour. — J. Res. Lep. 23: 125-142.

SalehialaviY.FritzscheK.ArnqvistG. (2011). The cost of mating and mutual mate choice in 2 role-reversed honey locust beetles. — Behav. Ecol. 22: 1104-1113.

Solomon-LaneT.K.WillisM.C.PradhanD.S.GroberM.S. (2014). Female, but not male, agonistic behaviour is associated with male reproductive success in stable bluebanded goby (Lythrypnus dalli) hierarchies. — Behaviour 151: 1367-1387.

SorensenP.W.PinillosM.ScottA.P. (2005). Sexually mature male goldfish release large quantities of androstenedione into the water where it functions as a pheromone. — Gen. Comp. Endocrinol. 140: 164-175.

SteeleM.A. (1997). The relative importance of processes affecting recruitment of two temperate reef fishes. — Ecology 78: 129-145.

StiverK.A.AlonzoS.H. (2009). Parental and mating effort: is there necessarily a trade-off?Ethology 115: 1101-1126.

SukH.Y.ChoeJ.C. (2002). The presence of eggs in the nest and female choice in common freshwater gobies (Rhinogobius brunneus). — Behav. Ecol. Sociobiol. 52: 211-215.

SvenssonP.A.ForsgrenE.AmundsenT.SköldH.N. (2005). Chromatic interaction between egg pigmentation and skin chromatophores in the nuptial coloration of female two-spotted gobies. — J. Exp. Biol. 208: 4391-4397.

SwierkL.MyersA.LangkildeT. (2013). Male mate preference is influenced by both female behaviour and morphology. — Anim. Behav. 85: 1451-1457.

SymonsN.SvenssonP.A.WongB.B.M. (2011). Do male desert gobies compromise offspring care to attract additional mating opportunities?PLoS ONE 6: e20576.

TorricelliP.LugliM.GandolfiG. (1985). A quantitative analysis of the fanning activity in the male Padogobius martensi (Pisces: Gobiidae). — Anim. Behav. 92: 288-301.

TriversR.L. (1972). Parental investment and sexual selection. — In: Sexual selecion and the descent of man ( CampbellB. ed.). AldineChicago, IL p.  139-179.

TrunzerB.HeinzeJ.HölldoblerB. (1999). Social status and reproductive success in queenless ant colonies. — Behaviour 136: 1093-1105.

Van BelleS.EstradaA.ZieglerT.E.StrierK.B. (2009). Sexual behavior across ovarian cycles in wild black howler monkeys (Alouatta pigra): male mate guarding and female mate choice. — Am. J. Primatol. 71: 153-164.

van NoordwijkM.A.van SchaikC.P. (1999). The effects of dominance rank and group size on female lifetime reproductive success in wild long-tailed macaques, Macaca fascicularis. — Primates 40: 105-130.

VoigtC.GoymannW. (2007). Sex-role reversal is reflected in the brain of African black coucals (Centropus grillii). — Dev. Neurobiol. 67: 1560-1573.

WestneatD.F.SargentC.R. (1996). Sex and parenting: the effects of sexual conflict and parentage on parental strategies. — Trends Ecol. Evol. 11: 87-91.

WileyJ.W. (1976). Life histories and systematics of the western North American gobies Lythrypnus dalli (Gilbert) and Lythrypnus zebra (Gilbert). — San Diego Soc. Nat. Hist. Trans. 18: 169-183.

YoungA.J.CarlsonA.A.MonfortS.L.RussellA.F.BennettN.C.Clutton-BrockT. (2006). Stress and the suppression of subordinate reproduction in cooperatively breeding meerkats. — Proc. Natl. Acad. Sci. USA 103: 12005-12010.

ZoranM.J.WardJ.A. (1983). Parental egg care behavior and fanning activity for the orange chromide, Etroplus maculatus. — Environ. Biol. Fish. 8: 301-310.


  • View in gallery

    Scenarios and rules for scoring courtship solicitation postures by Lythrypnus dalli females (top views). The body of the female (♀) should be aligned perpendicular to the male (♂) so as to display the state of her distended abdomen (gravidity) to the male, the female must remain stationary and not engaged in interaction with another individual or feeding. (A) The female could be positioned anterior or (B) posterior to the male; (C) some part of the female body must be intersected by the median linear axis of the male.

  • View in gallery

    Social groups of Lythrypnus dalli show within and between group natural variation in (A) mean total number of eggs (orange + eyed) laid on 8 different days; (B) mean number of nest care (fanning and rubbing) bouts exhibited on 8 different days during 10 min observation sessions, over the course of 26 days in social groups housed in a semi-natural laboratory environment. Each social group (N=16) consisted of one male and two size-mismatched females. Error bar for each group captures variation across time; Group 1 did not have any eggs during the experimental period.

  • View in gallery

    Effect of egg presence on behaviour exhibited by male Lythrypnus dalli during 10 min observation periods over a 26-day period (A) rates of male approaches towards females; (B) number male nest care bouts (fanning and rubbing); (C) nest care duration. Each group comprised of one male and two size-mismatched females. Eight behavioural observations were conducted for N=16 groups. Data are means ± SEM.

  • View in gallery

    Effect of egg presence on rates of courtship behaviour exhibited by Lythrypnus dalli living in groups comprised of one male (♂) and two size-mismatched females (α♀, alpha female; β♀, beta female) during egg absence and presence over a 26-day period. Courtship behaviours quantified were jerks for males and solicitations for females. When there are no eggs in the nest, rates of beta solicitations are higher than males jerk rate. Eight behavioural observations were conducted for N=16 groups. p<0.05. Data are means ± SEM.

  • View in gallery

    Relationship between number of eggs and male Lythrypnus dalli behaviour exhibited during 10-min observation periods over a 26-day period (A) Total number of eggs (orange + eyed) and number of nest care bouts (fanning and rubbing); (B) total number of eggs (orange + eyed) and rate of male courtship jerks; (C) total number of eggs (orange + eyed) and rate of male approaches towards females; (D) number of eyed eggs and number of nest care bouts (fanning and rubbing); (E) number of eyed eggs and rate of male courtship jerks and (F) number of eyed eggs and rate of male approaches towards females. Eight behavioural observations and 8 egg counts were conducted for N=16 groups over a 26-day period.

  • View in gallery

    Relationship between number of eggs and rates of female Lythrypnus dalli behaviour exhibited during 10-min observation periods over a 26-day period (A) Total number of eggs (orange + eyed) and rate of alpha female solicitation; (B) total number of eggs (orange + eyed) and rate of beta female solicitation; (C) total number of eggs (orange + eyed) and rates of alpha female + beta female solicitation; (D) number of eyed eggs and rate of alpha female solicitation; (E) number of eyed eggs and rate of beta female solicitation and (F) number of eyed eggs and rates of alpha female + beta female solicitation. Eight behavioural observations were conducted for N=16 groups over a 26-day period.

  • View in gallery

    Simplified flow chart showing the pattern of interactions within Lythrypnus dalli groups consisting of one male, an alpha female, and a beta female, based on first order Markov transitions. A total of 875 transitions were used to generate the chart, and arrow thickness is proportional to the frequency (converted into percentage, and noted beside the arrow) of the transition. To reduce complexity, only frequencies > 0.1 (10%) are shown. Abbreviations: ♂, male; α♀, alpha female; β♀, beta female; A, approach; D, displacement; S, solicitation; I, interruption of solicitation.


Content Metrics

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 34 34 10
Full Text Views 71 71 61
PDF Downloads 3 3 1
EPUB Downloads 0 0 0