Extra-pair mating in a socially monogamous and paternal mouthbrooding cardinalfish
Item Type Article
Authors Rueger, Theresa; Harrison, Hugo B; Gardiner, Naomi M; Berumen, Michael L.; Jones, Geoffrey P
Citation Rueger T, Harrison HB, Gardiner NM, Berumen ML, Jones GP (2019) Extra-pair mating in a socially monogamous and paternal mouthbrooding cardinalfish. Molecular Ecology. Available: http:// dx.doi.org/10.1111/mec.15103.
Eprint version Post-print
DOI 10.1111/mec.15103
Publisher Wiley
Journal Molecular Ecology
Rights Archived with thanks to Molecular Ecology
Download date 02/10/2021 15:36:31
Link to Item http://hdl.handle.net/10754/631945 This article isThis article by protected copyright. All rightsreserved. 10.1111/mec.15103doi: to lead copyediting, paginationbeen throughthe andproofreadingtypesetting, process,may which This article acceptedhas been for publication andundergone fullpeer review buthasnot mouth brooding, mouthbrooding paternally long have that confirmed studies bond have pair monogamous form vertebrates Many Abstract addressed: be email: should theresa.rueger@ to whomcorrespondence Author * Abdul 3 Australia 4811, Queensland Townsville, 2 4 Townsville, 1 P Jones Rueger*Theresa cardinalfish E Article : Original Article type 0000 ID : (Orcid BHARRISON HUGO MR. 0000 ID: (Orcid RUEGER DR. THERESA Red Sea ResearchCenter, Red Sea University, James Cook Studies. Reef Coral for Excellence of Centre Council Research Australian University, JamesCook Engineering, and Science of College andAquaculture, Biology Marine Accepted Articlextra - . Social monogamy . Social term observations and genetic tools tools genetic and term observations increasingly increasingly lah University of Science and Technology, 23955 Technology, and Science of University lah -
pair mating inasocially pair mating differences between the of thisversion citethisarticle and asVersion Record.Please 1, 1, 2
811 QLD, Australia. 811
is thought to be associated with a high degree of confidence in in paternity confidence of degree ahigh with associated be is thought to shown that many offspring arise from mating arise from offspring shown thatmany 1, 1, 2 , HugoB Harrison is relatively common is relatively
cardinalfish, Biological and Environmental Science and Engineering Division, Division, Engineering Scienceand Environmental and Biological
monogamy monogamy extra or
monogamous and paternal mouthbrooding andpaternal monogamous Sphaeramia nematoptera Sphaeramia
were 2 s , NaomiM Gardiner
to mate to - - 0002
0001 in coral reeffishes, coral in applied to examine the examineto the applied - pair reproduction, either for males or females. Here females. or males either for reproduction, pair -
and and - 2105 8831 care - - 6900 Thuwal, Kingdom of Saudi Arabia Thuwal, Kingdom Saudi 6900 of - 6412) 0086) for
s their
1 . pair the monogamous of outside , Michael L , Michael Berumen
Paternal care in fishes Paternal in care but but
offspring parentage there there have been relatively few have beenrelatively .
However, genetic tools However, tools genetic
gmail.com of embryos in embryos of , s 3 . , Geoffrey, Two uch as uch
King King a - years years
This article isThis article by protected copyright. All rightsreserved. questioned. been has aremonogamous truly Clutton partners multiple abilityacquire to an individual’s limit that constraints ecological or care, biparental extensive for need asthe such constraints, life history on atleast for oneanother with mating exclusively pairs asheterosexual herein is defined Monogamy widespread gamete production theorised with females formand bonds pair systems, of mating agreat variety adopted Animals have Introduction Keywords of extra advantage group immediate from the individuals outside were fertil broods investment paternal high the females. Despite fromeggs two afemale by mothered were males,64 30.1% extra revealed parentage genetic However, observations of
Acceptede Article breeding cycle cycle breeding multiple partners partners multiple
cohesion - Brock2012) that : Monogamy, extra : Monogamy, than polyandry than
males have a greaterpropens a males have , confirmed that confirmed both males and females males females both and ised - pair mating opportunities. mating pair and a and (Wilson 1975; Wittenberger & Tilson 1980) &Tilson Wittenberger 1975; (Wilson .
However, in recent years the extent to which presumed monogamous species monogamous presumed which to extent the However, recent in years by twomales. by Extra (Breder & Rosen 1966; Emlen & Oring 1977; Smith 1984) 1977; & Oring Emlen1966; & Rosen (Breder s a result, s aresult, , where , - to varying degrees of varyingto degrees pair mating, parental care,Apogonidae parental mating, pair
S. nematoptera S.
polygyny females mate with several males males mate several with females group can maximise lifetime reproductive success by success by maximise lifetime reproductive can - - ity to mate with multiple partners partners matemultiple with to ity pair matings appeared to be opportunistic encounters with with opportunisticencounters be to appeared matings pair pair mating pair
,
that was not the the partner not was that inwhich . We argue that . that Weargue
form long promiscuity only malesonly by both sexes. Of 105 broods analysed fromanalysed broods 105 sexes.Of by both (Wittenberger & Tilson 1980; Lukas Lukas & 1980; &Tilson (Wittenberger - ranging ranging term pair bonds within within term bonds pair associated with with associated while
, . It
in which from have have is pair formation formation pair (Eml
and 11.5% of broods included included broods of 11.5% and th monogamy, ought multiple partners en & Oring 1977) en &Oring males and females engage females engage and males
due to the lower cost of costof lower the to due mouthbroodi to ariseto larger . contributes to It has been It has
in which which in when when group tak ,
is ng, 7. . ing there arethere more males males s.
6 % of This article isThis article by protected copyright. All rightsreserved. situatio extra reveal monogamy or confirmto genetic pairs lasting be filefishes et al. Thompson Hoese 2001; 1989) (Donaldson someof species and anemonefishes include examples Common smallcommonly species fis mostfor taxa. areunderstood poorly this behaviour in engage femalesmales to or either species monogamous ofextra levels high rule. the rather than exception Si previo than is more common reproduction pair on based 2003) non and seasons mating multiple of time,periods prolongedencompassing anotherfor one with associate females and males species, monogamous” ( “socially as described paternity. or maternity of or genetic evidence copulation of observations direct such llero hes
Accepted noextra and monogamous Article
based on based 2008 . g However, (Whiteman & Côte 2004) & Côte (Whiteman - n Zubiri Social monog Social mammals fish birds, and of species Most
where a male or a female produces offspri male produces afemale or where a prolonged association association prolonged Oxymonacanthus longirostris Oxymonacanthus ) ; . butterflyfishes butterflyfishes However, m However,
et al long ; . 1996; 1998) Hughes . 1996; studies enetic parentage - - damselfishes damselfishes term observations on the associat onthe term observations mating. pair coral crouchers coral crouchers , the proportion of offspring arising from arising extra of offspring proportion , the amy is relatively isrelatively amy et al.
closely associated with coral habitat coral associatedwith closely olecular analysis of broods of socially monogamous ofsocially broods of analysis olecular Chaetodon -
2007) pair matings pair This raises the question as to how pair bonds are maintained in face of in are maintained pair bonds how as to raisesthequestion This is , occurring in 14 of the most common coral reef fish families, families, fish reef in thecommoncoral 14 of most, occurring
Despite the Despite the - Dascyllus reproductive periods periods reproductive often often ; Caracanthus Paragobiodon sensu
widespread spp. unfounded (Barlow 1987)
and e and
have have have been observed been have spp. spp. Amphi
(Fric Whiteman & Côté2003 Whiteman increasing evidence increasing - pair xclusively mating with one partner seems to be the the be partnerseemsto one mating with xclusively usly thought thought usly (Fricke 1980) now now ke 1986; Hourigan 1989; Reavis & Copus 2011) Reavis&Copus Hourigan1989; ke 1986;
considered
p spp. mating
. rion in coral reeffish coral in
n
E spp g outside the matedpair the outside g ion between a male and a female, rather than by by than rather afemale, between amaleand ion ven in species with long with speciesven in shown shown . (Wickler & Seibt 1983; Whit 1983; Seibt & (Wickler (Wong (Wong
. In In spp
(Lassig 1976; Kuwamura (Lassig 1976;
remain Extra rare. many . (Westneat 1987; Moller & Birkhead 1994; 1994; & Moller Birkhead (Westneat 1987;
that ( to be to
Fricke & Fricke 1977; Buston 2003) Buston Fricke 1977; &Fricke ; (Barlow 1984, 1986; Thresher1984) 1986; 1984, (Barlow et al.
coral gobies coral gobies when males and females formed formed malesfemales when and
of these systems, mating mating theseof systems, theof assumption for extra
monogamous
es - 2005) ). pair mating and the propensity of propensity mating the and pair
compared to other other marine to compared In sociallymonogamousIn - ; pair mating in socially socially in mating pair hawkfishes hawkfishes Gobiodon - . pair mating describes a describes mating pair
- In In coral term bonds pair Such species are best species Such
A were classified canthochromis et al. genetic genetic eman & Côté Côté eman & reef fish species reef fish
spp Cirrhites
1993 appears to appears to .
monogamy (Cole & ; Wong ; Wong , most
extra
as spp. spp.
; ; .
and
- This article isThis article by protected copyright. All rightsreserved. Accepted paternal monogamous, 1999). Variabilich zebra Pseudotropheus observed been has paternity than eggs more produce can they when seekextra to a greater femalespropensity having with limited, be may Avis ha males that other probability 1985) Gross &Sargent 1979; &Zaret Perrone probability is ahigh externally in paternity in confidence to relate isthought care Paternal qua high is of one mate just which acquiring of benefits Article the increases and mates, sequester multiple to opportunity males may limit the expenditure energetic as body mouthbrooding the embryos on substrate, developing guarding care. mode the parental on of depend matings. monogamy genetic extra of result allelesfound number of the on based mating of out onebrood young, hatched of care biparental polyacanthus e 1997b) However, the relative frequency of multiple mating by males and females in socially socially in males females by and mating multiple of relativefrequency the However, factorsaffectin The in
pipefishes and seahorses seahorses pipefishes and romis moorii , a species without a larval alarval phase and ,without aspecies . W - pair mating activity eithersex. by activity mating pair hen requires detailed genetic studies that measure the prevalence of of measure prevalence the that studies requires genetic detailed
that
males have all the parental care duties, opportunities duties, care parental males allthe have
- (Parker & Kornfield 1996) &Kornfield (Parker caring coral reef fishes has not been examined. been not reeffisheshas coral caring
(Sefc males are genetically related to the offspring they carefor they offspring the to related males genetically are g opportunities for extra for opportunities g in fish with a range of mating systems including systems including withmating of fish in a range d et al.
fertilised fertilised
(Perrone & Zaret 1979) &Zaret (Perrone 2008) Monogamous f Monogamous a single a single the eggs a eggs the , and the mosquito fish the mosquito , and (Miller . male ca However, t However,
Distinguishing between social monogamy and and monogamy betweensocial Distinguishing ,
Protomelas spilopterus one of only afew only one of 30 nother - - pair mating in monogamous fishes are likely to likely are monogamousin fishes mating pair ishes often exhibit paternal care, either by paternal care,by either exhibit ishes often Sims
was concluded n care n for lity lity
et al. male is caring for for caring male is his would only apply ifapply only wouldthere his (Barlow 1984; Whiteman & Côte 2004) WhitemanCôte 1984; & (Barlow . In speciesIn
,
or by carrying the embryos o the embryos carrying or by 2008)
Gambusia holbrooki Gambusia (Clutton
reef fish species known to have have to known species reef fish
to show evidence extra of show to . -
pair copulations, especially especially copulations, pair Such mixed broods may be the the may be mixedSuch broods with paternal broodcare paternal with - fertilising
- for extrafor (Kellogg et al. 1998), and and et al.1998), (Kellogg Brock Brock 2009) (Smith 1979; Jones& (Smith1979; the the cichlid fishes, - pair and and pair (Blumer 1 pair fertilizations pair
(Zane et al. (Zane et . Multiple s
were wh extra n the the n ere there 979; 979; a low low a , the , the - pair - pair .
This article isThis article by protected copyright. All rightsreserved. mouthbroo that hypothesis in this monogamy species social of occurrence and males derivedfrom be would offspring of analys parentage fromor paternity maternity multiple genetic either provide extra absence of doesnot monogamy social However, data alone. on behavioural based be monogamous pairs size form assortative to prolonged, found cardinalfish, pajama and extra pair of examine extent the reproduction. a condition physical andincrease their cannibalisebroods to possibility the Takeyama faster eggs produce females can for potential isthe There paternity. in confidence of degree the with associated paternal care is level of ahigh whether of test auseful provides mouthbrooders extra behaviour. reproductive 2007) 2000) spawning cyanosoma notatus with monogamy l.
Accepted Article 2007) - pair mating pair ). the most For part , Cheilodipterus quinquelineatus Cheilodipterus
d (Kuwamura 1 The aim of this study was to combine wasto along study aim this The of of avariety exhibit mouthbrooding cardinalfish Paternally
. the opportunity to sample clutches of developing embryos and determine the presence of of presence the determine embryos and developing of to sample the clutches opportunity
( Genetic studies can reveal the extent to which both sexes are involved inextra sexes are involved whichto both extent Genetic canreveal the studies et al. Apogon niger Apogon
(Rueger (Rueger
-
2007) lasting pairs, lasting pair matings. matings. pair has et al. Sphaeramia nematoptera Sphaeramia
983, 1985) 983, not been described in cardinalfish. cardinalfish. in not beendescribed . On the other hand, e hand, other On the There have been no no There been have
, (Kuwamura 1985)
2014) these mating systems have been established by direct observations of observations direct by established been have systems matingthese ding is associated with a high level of confidence in paternity in confidence level of a high with isassociated ding
which stay together for entire breeding seasons or longer longer seasons or for breeding entire together stay which The The
) than males can brood males canbrood than , ;
Pterapogon kauderni Pterapogon to promiscuityto small group sizes and sizesand group small - pair mating in the pair matingin
(Kuwamura 1987) , xtra genetic studies on on studies genetic Ostor .
females in pairs, as this w asthis pairs, in females (Rueger (Rueger (Rueger (Rueger Since male and female Since female male and -
pair mating by males could be expected because of of because expected be males could by mating pair with transient pairs, which split up shortly after shortly split up which pairs, with transient hinchus doederleini hinchus - term behavioural study with genetic tools to to genetic tools with study term behavioural them
socially monogamous, paternal mouthbrooding mouthbrooding monogamous, paternal socially
(Vagelli & Vo & (Vagelli et al. et al. Applying genetic studies to patern to geneticApplying studies paternal mouthbrooding paternal , Apogon imberbis (Okuda 1999; Okuda Okuda 1999; (Okuda extra
2016b) 2016b)
socially monogamous species and monogamousand socially species - pair mating females by pair mating systems, from e , the species would be assumed to assumedto be would species , the
s. and would support the would support and lpedo 2004) lpedo
S. nematoptera S. We (Kuwamura 1985; Okuda 1985; (Kuwamura ould be with be consistent ould
(Okuda 1999; Takeyama (Okuda 1999;
predicted that the majority majority the that predicted
(Klein & Raventos & Raventos (Klein
et al. in in , Ostorhinchus Ostorhinchus S. S.
have been have
nematoptera 2 ( . ensure - Apogon Apogon 003; 003; ,
pair
social since since al
the the
the the et
This article isThis article by protected copyright. All rightsreserved. taken. DNA tissue samples and weretagged 22groups the each of within All individuals Accepted of casethis allcolonies individuals). (N =544 oil July was collected formation social pair data and observational re information viaand visualcensus, days analyses millimetre the nearest to measured fish allwas of length 2000) years, lastfor to shown VIEbeen onfish. has the five and positions colours tags (VIE) Elastomer Implant males brooding carried by embryos from father and groups Article potential identify two years to for ofcardinalfish tagged groups We observed mating behaviour and formation Pair periods resting diurnal during remain pairsthat female male formand adults 1). from 20 October 150°05’E), (5°30’S, NewGuinea Papua Kimbe Bay, Centre, Conservation and Research NaDari reefsnearMahonia inshore on wasconducted study The species siteand Study Methods (Munday (Munday & Wilson Here, -
.
August 2013, March 2013, August and does impact and not
All fish tags in this study remained clearly visible over the twothe visible over remainedclearly this study tags in All fish and contrasted our observations with genetic parentage analyses to identify the true mother mother true identify the to analyses parentage withgenetic observations our and contrasted Observational studies were conducted October conducted were studies Observational . During each of the five observational periods all individuals were located every two to three three two to every located were periods allindividuals observational thefive eachof . During Sphaeramia nematoptera Sphaeramia
A group is defined as an aggregation of fish on a distinct patch of habitat, in in habitat, of fishpatch adistinct of on as anaggregation is defined A group 1997) Porites cylindrica - cardinal April 2014 and 2014 April
and hand nets, from 22 groups of fish located across five different reefs different five of fishacross located groups nets,fromand hand 22 (Northwe (Rueger
fish behaviour nor affect susceptibility to predation topredation nor affect susceptibility behaviour fish is common where it is common where
et al. st Marine Technology) Technology) st Marine . corded on the on corded
Groups varied in size from 4 to 32 individuals individuals 32 varied sizefrom in to Groups 4 in September 2014. Septemberin 2014.
2016a; b) 2016a; very close to each other, and have high sitefidelity, have high and eachother, to close very . . All fish were physically marked using Visible using marked physically were All fish .
- ir lives in small groups, within which most withinwhich small ingroups, lives
and and November 2012, February February 2012, November
most likely mate. Overall, 500 hours of 500 mostmate. Overall, likely over 24 over caudal
with unique combinations fromsix combinations with unique Fish were caught, using diluted clove clove diluted using Fishwere caught,
months. fin clips taken clips fin at least - 12 to September12 to 2014
year period. year
several months several pair bonds within the within pair bonds
for genetic genetic for The standard The -
March 2013, March 2013, (Marnane (Marnane
(Figure 1). (Figure 1).
, often (Figure
This article isThis article by protected copyright. All rightsreserved. the 24 within were recorded groups movements between to 25were fish, overfound of 544 Out between groups. fish movements of afewrecorded only were There stable. was relatively groups of Membership time. across observed were henceforth pairing of andincidences theirlocation tagged and and caught th manner, this in appeared fish new When elsewhere. aggregations area unsampled from adult reefson the five groups observed All sampling. and observation breeding the in theywerepairs, included breeding formed throughout observed were juveniles Tagged frombehaviour un signsof breeding and any location (Rueger ma the with females remain the cycles, and multiple brooding represents which months, together after4 found were pairs 50% month, of atleast for one together pairs aretypically al. c in tooccur known isnot change (female). Sex before brooding abdomenbulging shortly (male) brooding and during buccal cavity distended the observing by wasdetermined Sex be heterosexual. to all were and found pairs defined 5 on be observed pairswhich would during days, 14 approximately lastfor cycle Abreeding sitefidelity. high have and ove another one to
Accepted Article 2012) S. S. nematoptera up broods. males and taking mating toobserve courtship, regularly monitored Pairs were fish two when determined Pairs were et al. . Our previous
2018) - 7 separate occasions 7 r one or more breeding cycles or morebreeding r one .
during the 24 during the
work has established that the species appears to be socially monogamous as monogamous socially be to appears the species that established work has where sampled thoroughly, although the rare appearance of new, untagged, untagged, new, of rarethe appearance although thoroughly, sampled where ardinalfish -
month study period might suggest there was movement into the the movement into might was there period month suggest study . Courtship behaviour was only ob wasonly behaviour Courtship
the observational periods observational the (Kume
were consistently observed in close proximity (≤ 20cm) closeproximity in observed were consistently . Pairs typically rest within the same the coral branches within rest typically . Pairs et al. et - paired paired
switch groups permanently and a total of 91 91 atotal of and permanently switch groups -
month period. month period. 2000a; Pisingan & Takemura 2007; Choi Choi &Takemura Pisingan 2007; 2000a; tagged individuals were also monitored. monitored. also were tagged individuals
. If juveniles matured and matured and juveniles . If served between partners thus thus between partners served
les during brooding brooding during les ey were
The et This article isThis article by protected copyright. All rightsreserved. ±1.8 mean 15.1 of a with the R package in binsets usingmarker distinguished alleleswere Unique (Applied Biosystems). v4.0 Genemapper DNAanalyse ABI 3370xl an on the using Type wereamplified Loci mismatchbetween ratio as the calculated and fromindividuals repeat samples 43 using wasassessed error Genotyping in described procedures the PCRs following multiplex four markers in Nucleospin the using 95%ethanol in preserved samples tissue from fin wereperformed DNA extractions 2000) A a sample of (p=0.5), clutch n≥ln(0.05/ln(1 if certainty size of arandom sample theory that predicts mass. probability egg Binomial congealed the centreof the eggs the extracting assayed. theseclutc of males.each 64 From few nets and hand collected were males observed different groups. among or within females and males broo carried by analyses genetic and DNA sampling
Acceptedsample of Article minutes n
. will include eggs from a female which laid some proportion some proportion laid which from a female eggs will include
We undertook genetic parentage analyses to identify the true mother and father from embryos from father and mother true the identify to analyses parentage genetic We undertook To To - 96 Tissue kit (Macherey kit Tissue 96 . consider 10 eggs eggs 10 105 clutches clutches with 105
diluted clove oil. diluted ding males. From these analyses, we measure the frequency extra of frequency the wemeasure analyses, males. Fromding these es in alleles and the number of replicated alleles alleles numberreplicated of the allelesand in es from
would be would the possibility of multiple mothers in each clutch, eachclutch, mothers in of multiple possibility the MsatAllele different parts of the egg mass, including several points on the surface and surfaceand the on several points mass, egg including the of parts different
SE - p) p) five , in this population of this population , in (Ross 1997)
considered sufficient to detect a proportion of 0.25 of detectaproportion to considered sufficient (n = 64 brooding males). To do this do males). brooding To =64 (n
approximately approximately eggs would be sufficient to include at least one egg from each mother. from each egg least at sufficientinclude one to be would eggs r (Applied Biosystems), and individual genotypes were scored in in scored genotypeswere individual and r (AppliedBiosystems), Males would usually expel usually Males would hes,
-
(Alberto 2009). 2009). (Alberto it Microsatellite PCR kit (Qiagen), PCR products were screened were screened products PCR (Qiagen), kit it Microsatellite PCR - Nagel). All individuals were genotyped at 23 microsatellite microsatellite at23 weregenotyped individuals All Nagel). 5 - 20 . If two mothers have an equal number of embryos in a embryos of number equal mothersan two have . If
embryos were subsampled. embryos were subsampled. 6000 S. nematoptera - A range of of A range 10000
Within the study periods, all broods found in found in study all broods periods, the Within
embryos the brood the
3
to
(Supplemental Material Table 1). 1). Table Material (Supplemental , p (Pompan
brooding brooding
34 alleles 34 in total in of eggs int eggs of , either Rueger Rueger embryos In total 1056 embryos totalwere 1056 In
on etal on were collected immediately or or immediately males was et al. he nest, with 95% 95% with he nest,
were sampled were
(DeWoody & Avise (DeWoody observed -
. were caught were pair mating by pair (
2005) 2015 - specific specific ) . . from the from the
per locus per within within
by by
with a
, This article isThis article by protected copyright. All rightsreserved. Accepted exacttest. Fisher’s reefs using the of instances behaviour, tell wecould as far from outsid study the thesampled fish in oneof werenot because they known, different a came from they whether whether We determined extra and Pair offspring include type assi being offspring simulated of withmostparents accuracy, describedHarrison in methods following Article Mykiss simulated in Apopulatio COLONY settings. of accuracy the assess to testwasconducted Asimulation theanalysis. in polygamous considered sexes were both and parents as candidate females wereincluded and males putative All threshold. probability fullthe using performed were Analyses malecardinalfish. eggscarriedby of mothermothersaselection or of the most likely identify softwareCOLO the with conducted were assignments Parentage error of 2.2 average an genotyping had 19 loci remaining markers Four ±0.058 0.733 ±0.060 was0.666 heterozygosity meanThe observed - I error I error d
more than one genetic father or mother. more genetic or father one than held in heldin e of the study area. study S the of e 0.
SE. 1 that that - %, type pair matings within and among and among matings within pair another males’ buccal cavity. cavity. another buccal males’ Significant deviation from Hardy from deviation Significant showed high genotyping error (≥6%) error were genotyping showed high (Kalinowski 2009) (Kalinowski ,
- during during II error II error extra extra - the two the pair
0 - ampling of of ampling %) pair mating pair male . group Multiple matings were defined as clutches of embryos embryos of as clutches weredefined matings Multiple -
year -
to to a with medium precis method likelihood parents et al .
measure the frequency of type I and type II errors anderrors I II type type of frequency measure the I n cases where the cases the n where study period study n of 1000 offspring and 250 mothers and fathers was fathers was mothers and and250 1000 of offspring n resident resident
were compared between were between compared .
(2013). The parameter set yielded the highest overall overall highest the parametersetyielded The (2013). group
were Extra - Weinb individuals individuals
s p SE and SE
- art of the same the art of pair males pair . To check for any locational biases in mating mating biases locational in any checkfor . To % erg equilibrium was found in found was equilibrium erg
±0.4
gned to the correct parent pair correctparent the to gned excluded excluded mean expected heterozygosity was meanheterozygosity expected extra
within the study study withinthe area NY v2.0 NY v2.0 SE
, we deemed them to be be them, we to deemed were defined as a were defined - . pair individual pair
groups on the same or different different sameon the or groups group from the analyses. The The from analyses. the (Jones & Wang 2010) (Jones &Wang
as the breeding pair or pairor as thebreeding ion, long run and low runlow long and ion, ’ s ny identity identity was not was was
male four complete, complete, migrants
that (
that 99 loci. loci. .
9 to
sired %; This article isThis article by protected copyright. All rightsreserved. Accepted completely buccal cavity asingleclut brooding, towards them. During aggressive behaviours displaying considerable time partners matingspending both the tomating with close stay pair, to observed e amating When 2000). (Marnane cardinalfish reefdwelling coral otherspeciesof in observed been has similar what to nematoptera wi buccal in his cavity clutch up the scoops and moves back then maleThe malequivers. the clutch,during which buoyant a cohesive, neutrally drops female The fin. twi side and s perform males females and Both branches. happen active courting between pairs observed wereonly displays Mating observations Mating Overall, Article the the of malein position in changes social with aspaired identified be could events mating of 70 in brooding to weeksprior four for pairswasavailable social on data Behavioural periods observational placebetween taken times three the to over one Each monogamy Social Results of the 105 the of partner
20 pairs 20 tching pectoral fins. Males and females line up side by side and the male flicks his caudal caudal the male his side byand flicks up females line Males and fins. pectoral tching
typically begin to move out of the coral colony to migrate to their nightly feedingsites, nightly migrate their to coralcolony movethe to outbegin of typically
. I could be identified be could n 94.3% (66 of 70) of casesof 70) (66of 94.3% n clutch vent is occurring however, conspecifics as well as other cardinalfish species werespecies cardinalfish other as aswell however, conspecifics occurring is vent were
es ed observed to produce multiple clutches during th multiple during clutches produceto observed
represents one successful mating event, with each male witheach event, mating successful represents one (Kume starting at dusk and throughout nightfall. Mating t Mating nightfall. throughout and startingat dusk two -
year year . In these cases, partners could not be identified not be could these . In cases, partners et al. a
social partner. In the other four cases males were males observed four cases theIn other social partner. study p study group
2000) .
where behavioural dataavailable was behavioural where - or due to lack of to due lackof or . eriod
bends and males/females display by presenting their by presenting display males/females and bends Brooding in in Brooding , although other mating events events othermating , although
and occurred throughout the day, although most although theday, throughout occurred and S. nematoptera S. consistent consistent
thin seconds. During nightfall, During thin seconds. e study proximity to anyfemales to proximity
lasts for 8 days and happens andhappens days 8 lasts for akes .
ch fills the male’s male’s the ch fills
are likely to have are likely place within coral coral place within due due observed observed , the brooding males brooding , the to f to the the requent brooding 105 ,
but no but no S. S. .
This article isThis article by protected copyright. All rightsreserved. during Ofthe sampled population. the of part Extra extra complete or partial malessocial in Clearly, socialpair. its than from other clutch afemale an entire remaining was which between embryos differences morphological clear had theseclutches of One clutch. the of (±7.3%) b each In twodifferent females. by mothered were females femaleand of progeny werethe clutches (69.7%) 46 social pairs, clutches fromknown 66 Of the cycl breeding adifferent femalein another with be brooding to were which found two of sampled population, non eight ofthe Four 2). Table Material (Supplemental non average, On loci. multiple mismatches at thebasis of on excluded were all cases, sires In male1). (Table brooding the than amaleother by been fathered had that someeggs contained (7.6%) but clutches 8 (92.4%), clutche 97 in male thesolefather was that brooding the Wefound eggs. of clutches 105 of parents the mothers, we identified and putative embryos males, on brooding analysis parentage genetic Using e and Pair per clutch month one maximum of year Accepted to elonging Article - in fact merged frommerged fact in round. Males have been observed to brood two clutches in one month, however, brooding a brooding month, however, one in two clutches brood to observed been Males have round. -
pair mating by females was also found. Seven of Seven the found. was also byfemales mating pair yolks were of different colour correspond colour were different yolks of the sampling period (Table 1). (Table samplingthe period ,
demonstrating evidence of extra evidenceof demonstrating
xtra 13 (19.7%) 13 clutches
(Table (Table
the extra e. - pair
- brooding males sired 18.4% (±2.1%S 18.4% sired brooding males 1). 1).
mating - In the other 20 clutches 20 theIn other pair female ranged from female ranged pair - two clutches and and clutches two pair mating. mating. pair
with extra with was
se
more c ,
- 2 - pair mating by male cardinalfishes. Seven of these of Seven malemating by cardinalfishes. pair pair matings by the malethe matings by pair the result of separate matings resultofseparate the
females ,
ommon males were carrying eggs mothered by different different by mothered eggs males werecarrying 10 ing ing of theseof seven - 80% , which produced 2 clutche 2 produced , which to the different mothers to thedifferent
in the study population the in - E) of the analysed embryos in these clutches theseclutches in embryos analysed the E) of
partner males could be identified as part of the the of aspart identified be could males partner of sampledof extra
case - pair ,
emb s, the brooding male was carrying carrying brooding malethe was
females could be identified to be be to identified be females could
the the ryos with a mean of 32.1% with 32.1% amean of ryos on differentdays on proportion proportion , indicating that , indicating . s
,
pairs take part in in part pairs take were of embryosof the male paired in asoci in . In . In
this clutch
(10.6%) (10.6%) the the al pair s , in , in This article isThis article by protected copyright. All rightsreserved. observations confirm of one McCoy 1991; Brock pre isa monogamy that assumptions held long contradict the observations other males. These by fertilised also immediate their within females separate fromtake multipleclutches to were shown offspring of majority the predicted, mating exclusive indicates These provide embryos The exact, p=0.579). pair inhabiting error. genotyping to due possible 17 remaining distant pair mostIn cases extra and Pair Discussion
Accepted- Article requisite in the evolution of parental care systems that that parental care evolutionof systems the in requisite males and 20 extra 20 and males combination of of combination between nor p=0.547) exact, (Fisher’s sampled five reefs between the matings mated with females from other groups. groups. mated females fromother with findings demonstrate that neither social monogamy nor high monogamy nor social neither that demonstrate findings the firstthe group
, however unlikely, unlikely, , however that mating systems may be much more complex than more than much be complex may systems mating that the
. s with one male from one s with
extra
extra small area - cases of cases of pair matings within and among and among matings within pair d
unique insight into the reproductive strategies in a mouth a in strategies the into insight reproductive unique - - pair partners pair pair partners pair observations of social pair formation and theand ge formation pair social of observations
et al - concrete pair females
It thatescaped fish is unlikely was .
, 2001
since both that individual that
thorough , Sheldon 2002, , Sheldon
did not belong toanysamplednot did belong evidence of of evidence were from a different were adifferent from a (
, only nine (32%) were from the same were (32%) the nine from , only 70 group
males and females took part in part took males females and . %) There were no locational differences in the numberof the in differences locational wereThere no
w 80m away parentage We also found cases where males carried eggs that were that males eggs carried caseswhere found We also ere extra group
Kokko and Jennions 20 Kokkoand from mated pairs. However, However, matedpairs. from - pair mating in a in mating pair
s
could not be matched be not could and afemale and
group from have a high cost to eitherto parent cost ahigh have observation as sampling of as sampling observation
than the breeding pair. thebreeding than
expected based solely on on solely based expected group - monogamous monogamous from agroup investment mouth investment netic parentage analysis of analysis netic parentage
extra (13 females,(13 08 ) - group . These findings provide . Thesefindings to known groups members groups known to pair matings. As was As matings. pair - brooding brooding 9% of 9%
. werefrom Two 330m coral reef fish and and coral reeffish
4 group brooding brooding males group
Of the Of the males) - cardinalfish brooding
away known behavioural behavioural s (Fisher’s s (Fisher’s
and (Clutton 8 . . The . The It is It extra extra 21% group . -
- - s
This article isThis article by protected copyright. All rightsreserved. Accepted male brooding pipefish (Takeyama restricted is normally when periodfeeding the mouthbrooding during condition maintain to males described to up take at least partially, eggs, female’s paired carriedbeing number embryos of However, take fromfemales. more eggs potentialto other the have somesmall that apair in them canbrood males the quicker than eggs that males Our 2008) 2 mother, same sharethe inanest offspring Article monogamous cichlid socially speciesstudied the of almosthalf also occur the comparison, include with extra including strategies, mating complex and be deceiving studie detailed However, cycle breeding one last atleast to for isassumed monogamy pair lasting to bonds form found long been have coral reeffish extra of existence excludethe not monogamy does social Clearly,
study provides study social monogamy. In this In study monogamy. social .
d
,
S
either multiple females or or multipleeither females but also maximise their reproductive output by performing extra performing by output reproductive maximise their but also yngnathus in in are (Griffith e several species of cardinalfish of several species t al. t
already carrying eggs from another female. Female cardinalfish can potentially produce can potentially Female cardinalfish female. fromeggs another carrying already (Vincent
females lay small clutches females lay average proportion of extraof average proportion
2002, 2007) evidence evidence et al.
floridae
et al et s of other animal groups such as birds have shown that pairing behaviour can behaviour that havepairing suchshown as birds animalgroups other s of
2002)
. of (Jones & Avise 1997a) & (Jones
. Variabilichromis moorii Variabilichromis 2011) Multiple maternity has has maternity Multiple
. Inmammals an unusual female mati female an unusual
(Isvaran & Cl (Isvaran (Okuda 2001) (Okuda a female . ,
30% of broods 30% of
(Kolm 2001, 2002; Kume 2002; (Kolm 2001, (Okuda 1999, 2001; Kume 2001; 1999, (Okuda - -
10 fathers have been found in found fathers been 10 have (Okuda 1999) (Okuda pair paternity in in birds is 15%, paternity pair other than the s the than other ,
the equivalent extra equivalent the utton , it is, it additional additional , cared for by the paternal mo the paternal , caredby for
- where possible possible Brock 2007). In another teleost system, the teleost system,the another In 2007). Brock rarely rarely , both parents defend the nest and while all nestwhile the and parents defend , both ng strategy ng . This gives females the opportunity to be be to opportunity the . givesfemales This females do not do females eemingly established established eemingly - brood been describedbeen (Barlow 1984; Whiteman & Côte 2004) WhitemanCôte 1984; & (Barlow pair copulations, copulations, pair that the male cannibalises the socially socially the that malethe cannibalises
(Thresher1984) - - s , during which , during pair mating in coral reef fish. Many Many reeffish. mating coral in pair
group paternity exceeds 20% in in exceeds 20% paternity group . s F ince the buccal cavity limits the limitsthe cavity thebuccal ince et al. ilial cannibalism ilial cannibalism et al. -
pair matings. matings. pair
100% of though though remain 2002) , but isknown , but
2000b) are
an
, females partner. partner. uthbrooding fish, fish, uthbrooding often often d for many many species, for d so malesso rates of associ
, brood and has been has been associated associated It is possible possible It is
ated ated may allow may allow s
give In In for for up to up
(Sefc might might with the the with the the
eggs to to eggs 30% 30% et al.
.
This article isThis article by protected copyright. All rightsreserved. non among behaviour group non with mating of benefits genetic aneighbo with which produced is offspring extra compared to the within brood increasesand heterozygosity detection of risk reduces the male resident, extra of asaresult produced ofyoung 22% 2014) Jorgensen topromote cooperation thought unsampled pair same in heterozygosity E were found m In afew isnegligible. eggs extra costoftending the thus and is lower gobies Dewoody nest in occur by other males does contrast,cuckoldry By externally areclutches brooded the pipefish in even clutch, its bethesolesireof to has proven brooder the methods, withgenetic species surveyed allsyngnathid In pouches. brood or internal external in paternity Th paternity. fath brooding provide Here we xtra Accepted paternity ultiple Article males and females and males - gr
pair mating pair may ou (Jones (Jones oup
does seem to apply to to apply does seemto et , and even , and group
that the mated pair pair that mated the al. e idea that high investment, male paternal care is associated with the assurance of sole sole of assurance the with associated care is male investment, paternal thathigh e idea er. tweigh the possibility of cooperation and thus lead to higher rates of extra ratesof lead to higher and thus cooperation of possibility the tweigh et al. (Schlicht & Kempenaers 2013) &Kempenaers (Schlicht
1998; DeWoody DeWoody 1998; . Clearly, one of of one s. In s. In birds, mostextra However, exceptions exist exceptions However, S. nematoptera with individuals from a different fromadifferent individuals with may
2001) - then, neighbours. explain why the paternal care system paternalsystem care the explainwhy despite the
oral brooding by males does not e not bymales does oral brooding
and sticklebacks
only first example of of first example
the extensive sampling effort, effort, sampling extensive the occupied pipefish and seahorses pipefish and (Jones & Avise 1997a; Jones b, (Jones 1997a; &Avise
(Suter 10 . Relatively few instances of extra of few instances . Relatively et al.
An important gap in our knowledge that remains, is how mating is how remains, that our knowledge importantAn in gap - - 3 resident individuals and the avoidance of aggression within the the within aggression of avoidance the resident and individuals 0% of embryos were fathered by the the by were fathered embryos 0% of
2000a; Neff2004) 2000a; - et al pair mating is done with direct with mating isdone pair
( 10
- (Jones (Jones . ur ur pair mating were fathered by an unknown, or or non unknown, an by weremating fathered pair
: embryos %) 2007; Sardell a study on the bluetit, the on a study . Mating with non . with Mating (Foerster . In most instances, we could not identify identify not wecould most. In instances, et al. group fertilised
(Syngnathidae), in in (Syngnathidae),
et al. 1998) - ,
tending speciessunfish as such tending
may help maintain social stability and stability social may helpmaintain darters et al q uate with
persists 2003; Stapleton 2003; Stapleton which suggests which . In these. In
. by another male in the clutch ofa clutch malethe another in by
- et al 2010; Taff 2010; residents may bebeneficialbecauseit residents
(DeWoody (DeWoody - pair mating pair Cyanistes caeruleus Cyanistes . . In only 7.6% of broods 7.6%onlybroods of . In
1999, 2000; McCoy 2000; 1999,
S. S. nematoptera complete confidence in in completeconfidence territorial neighbours, is which neighbours, territorial Nerophis ophidion Nerophis systems, which extra
et al
they et al. et al. - . occurred
pair
paternal investment paternal males brood brood males 2013; Eliassen & Eliassen 2013;
belonged to belonged
2000b) 2007)
male. , the low rate of rateof low the - , found , found pair
(Gross 1991; (Gross 1991; the extra within the the within . Infish
, in which , inwhich
, sand et al
mating - - twosires embryos embryos
pair .
2001) that that ,
- the the .
This article isThis article by protected copyright. All rightsreserved. broods whole partialor for malecannibalise the to incentive an be then would which broods, their offer not femalesdo other that maleensure to brooding Barlow 1998) plentiful monogamousgoby, the In opportunities. mating at or cardinalfish thieves, egg male potential from the femalesprotecting the of in arole indicate may et al. S. mating pair extra by gained advantages many The 1999) theof populations pipefishes in found mating as to lead investmentit seemsto high availab are mature females However may ahig have group this females in broods, between phase alag have and brooding to during feed cannot themales since and polyandry may lead to teleosts, as proposed been care has parental system.mating Mutual to leadacomplex and malemouthbrooding by driven reprod higher equalor potential investment the male and high the of The a play to seems investment Parental for extra opportunity sites, whic theto feeding the during and migration night at pairs behave
every breeding cycle andpreventahigh to breeding every Acceptednematoptera Article
2016b) . In these systems however, . these however, In systems . Polygynandry mating opportunities for males create an advantage malesan advantage create mating opportunitiesfor ,
the male can offset the females the offset malecan the
shown in this study this in study shown one of the main drivers of monogamy in fishes, and paternal care, which is common in in is common which paternal care, and infishes, ofmonogamy maindrivers the one of . fem The . From the females’ perspective in in perspective females’ . From the other other have been found in pairs, most of which last for more than one breeding cycle cycle breeding one than more last for pairs, mostfound which in of been have - predators. Another reason to stay in a pair is to isto ens apair in reason stay to predators. Another pair mating outside the outside the mating pair , where ales stay with with the during males stay ales le
(Kume
both males and females acquire multiple partners, mating acquire females and males both (Whiteman & Côte 2004) (Whiteman& Côte raises multiple paternity
major et al her potential reproductive output reproductive her potential
- eemingly monogamous system with monogamous with system eemingly the question question the S. typhle S. pair mating and the occurrence of both male female both and of occurrence mating the pair and . ’
2000; Takeyama2000; role in shaping the reproductive system the shaping of reproductive in role advantage by cannibalising partial or broods or whole partial cannibalising advantage by - group quality partner from taking advantage of extra advantage of frompartner taking quality
and and S. nematoptera S. Valenciennea strigata Valenciennea
of why individuals pair at all. Most adults of adults of Most atall. pair individuals of why to occur.
S. floridae has not been described. has been not
the day while day the . Cardinalfish are paternal mouthbrooders, . Cardinalfisharepaternal
et al
(Manica 2002; Takeyama 2002; (Manica for
(Jones & , it is likely beneficial to stay with the the with stay to beneficial , it is likely . mate guarding mate guarding 2007)
brooding
than malesthan , abundant resources and and resources , abundant . Here ure a reproductive opportunity areproductive ure h mighth an represent
Avise 1997a; Jones 1997a; Avise uctive output output of uctive male and and male
, lasts
paternal care is such a such paternal is care by
(Okuda 2001) (Okuda
females ( pers such as such female S. nematoptera S. et al.
. has been has been
obs female (Reavis & (Reavis
extra -
other other . et al. 2007) pair ), which which ), , if , if (Rueger (Rueger extra . s
- are
pair . - . - This article isThis article by protected copyright. All rightsreserved. dataasso The Data accessibility A1847. manuscript. study.this reefsfor their to the Tamare We thank New Guinea. Papua Bay, Kimbe Centre, assistance. field for Noriega Smallhorn James Sih,Patrick White, Tiffany We thank Acknowledgement the matings of output extra in participate what abrood monogamyin social that show the with monogamy, genetic with congruent islargely monogamy social fish, reef coral confirms this for study that this conclude, To birds last long Furthermore,
Accepted Article clutches malestheir other fertilizing often
has been observed in birds and other and animals. birds in observed has been (Ismar
with extrawith
of of -
complex their own This study was conducted in accordance with JCU Ethics Committee, approval number approval Committee, JCUEthics with inaccordance wasconducted study This et al. et ciated with this study is available at Data Dryad isavailable atData study this ciated with -
pair matings pair 2010) - s mating systems pair matings. pair
. Molecular as well as long term behavioural studies are necessary to understand to are necessary studies termbehavioural aslong well Molecular as ing pairing .
We thank We thank Field work was supported by Mahonia Na Dari Research and Education Education and Mahonia by NaDariResearch work wasField supported
. Males which invest highly into offspring care seem into offspring to highly invest . Maleswhich bond
Females majority of offspring attributed to social partners. However, we However, partners. tosocial attributed offspring of majority
coral reeffish. coral s may benefit reproductive output, as known as known output, reproductive maybenefit four -
a caring reef fish does not guarantee exclusive mating, not guarantee exclusive does caring reeffish nd offset the females the offset nd
anonymous reviewers for helpful comments on the on comments helpful for anonymous reviewers clearly clearly
have the potential to increase their reproductive reproductive increasetheir to have thepotential We found evidence that both evidence thatboth found We - West, Mathew Vickers and Mariana Alvarez Mariana and Vickers West, Mathew ’ ,
- doi:10.5061/dryad.557br15 advantage
Kilu co Kilu mmunities for granting access granting for mmunities performing
males and males in several species of severalspecies of in
extra bear .
-
low levels levels low
pair females
similar to - This article isThis article by protected copyright. All rightsreserved. 161 h evidencefor and colonydemography morphology, Gonad Hoese DF(2001) KS, Cole Clutton Clutton orbicularis Sphaeramia cardinalfish orbiculate the of characteristics Reproductive SJ (2012) Heo HS, Park YU, Choi 146. 424, Nature, clownfish. in modification growth and size hierarchies: (2003) Social PM Buston N.Y.(NewYork). City, Press, Garden the NaturalHistory by History Natural of Breder CM 161. 54, 149 Biology, of Review Quarterly Fishes.The Bony the ParentalCarein Male (1979) Blumer LS 183 20, of Fishes, Biology Environmental monogamouscoralivore. a Spawni (1987) Barlow GW 767 Indo on Conference International Second Indo (eds.), & KMatsuura T Taniuchi RArai, Uyeno, freshwater monogamyamong of Acomparison (1986) Barlow GW 75 35, Fish Wissenschaft, für Archiv teleost fishes. monogamyamong of Patterns (1984) Barlow GW cited Literature ermaphroditism in ermaphroditism in
Accepted Article– – 123. –
775. 173. - -
Brock TH (2009) Sexual selection in females. Animal Behaviour, 77, 3 77, Behaviour, females. Animal in selection Sexual BrockTH (2009) care.Princeton parental of evolution The BrockTH (1991)
, Rosen DE (1966) Modes of reproduction in fishes. Published for the American Museum the Museum American for Published fishes. in of Modes reproduction DE (1966) Rosen ,
Gobiodon okinawae Gobiodon
in the Chuuk Lagoon, Micronesia. Fisheries Science, 78, 515 78, Science, Micronesia.Fisheries Lagoon, in theChuuk ng, eggs and larvae of the longnose filefish longnose andthe larvaeof eggs ng,
(Teleostei, Gobiidae). Environmental Biolo Gobiidae). (Teleostei,
Pacific Fishes, Ichthyological Society of Japan, Tokyo., pp. ofTokyo., Japan, Society Ichthyological Pacific Fishes,
Pacific Fish Biology: Proceedings of the Proceedings the of Biology: Pacific Fish
University Press. University and coral reef fishes. In: T. T. In: reeffishes. coral and – 194. Oxymonacanthus longirostris Oxymonacanthus
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11.
gy of Fishes, 61, Fishes, 61, gy of
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Accepted Article ( Darter ssellated . Evolution, 180252, . Evolution,
– 223.
– 747. Etheostoma olmstedi Etheostoma r Swimming and Mutual Partner Guarding in Monogamous Butterflyfish Butterflyfish inMonogamous Partner Guarding Mutual r Swimmingand
A Lepomis punctatus Lepomis 14) Extra 14)
– Joint Advertisement for Territory. Ethology, 73, 307 73, Ethology, Territory. for Advertisement Joint 1810. o gamy and sex change by aggressive dominance in coral reef fish. reeffish. coral in dominance aggressive change by andgamy sex –
569. - – pair mating and evolution of cooperative neighbourhoods. PLoS PLoS neighbourhoods. cooperative of and evolution mating pair 2128.
- ) assayed by microsatellite markers (Perciformes : Percidae). Percidae). markers(Perciformes : microsatellite by ) assayed pair matings. Nature, 425, 714 425, Nature, matings. pair – 302. Tactics in a Population of Redbreast Sunfish, Sunfish, Redbreast of aPopulation Tactics in
): Mate numbers and the influence of male reproductive malereproductive of influence the and numbers): Mate
-
dwelling hawkfishes (Cirrhitidae). hawkfishes (Cirrhitidae). dwelling
– 473.
males increase offspring males increaseoffspring – 717. a) The genetic mating a) The genetic
– 333.
Lepomis This article isThis article by protected copyright. All rightsreserved. 357 Accepted ( reversed pipefish AG,Rosenqvis Jones 52, 848 Evolution, Fifteenspine Stickleback. inthe Thievery Egg and AG,Ostlund Jones 6,203 Ecology, pipefish Gulf mating the the system in and ofmaternity analysis Microsatellite JC(1997b) AG,Avise Jones 1611 51, Evolution, DNAMarkers. Microsatellite Polygynandry JC(1997a) AG,Avise Jones 109 97, Naturwissenschaften, seabird. monogamous a socially costfor afitness replacement Mate entails (2010) ME BM, Hauber Stephenson C, Daniel Ismar SMH, R ARevolution Behavior: StudiesSocial in of Methods Field with Techniques Molecular Integrating C(1998) Hughes Article 61 Fishes,25, of Biology social systems. butterflyfish Environmental of (1989) determinants TF Hourigan Zool American Fishes. in Care Parental Male Female of Evolution and The RC(1985) Sargent Gross MR, 59 Sciences,332, Biological B: London of Society Royal the of Transactions Philosophical Sunfish. in MaleBluegill Selection Strategies: Reproductive Alternative Evolution of (1991) Gross MR 2195 11, Molecular Ecology, function. and adaptive variation Areviewinterspecific of birds: Extra in paternity pair (2002) Thuman KA OwensIPF, SC, Griffith Nature, – ogist, 25, 807 ogist, 25, 365. 266, 830 266, Syngnathus scovelli Syngnathus
– – 2 832. – 13. Syngnathus typhle Syngnathus - 822. nilsson S, Avise JC (1998) A Microsatellite Assessment of Sneaked Fertilizations Fertilizations Sneaked of AMicrosatellite Assessment nilsson Avise JC(1998) S, t G, Berglund A, Avise JC (1999) The genetic mating genetic systemasex The of A,AviseJC(1999) t G,Berglund
– esults. Molecular Techniques in Ecology, 79, 383 79, Ecology, in Techniques Molecular esults. 78. , a species with male with , aspecies –
66.
): a molecular inquiry. Behavioral Ecology and Sociobiology, 46, 46, Sociobiology, and Ecology Behavioral ): amolecularinquiry. in the Dusky Pipefish thein Dusky pregnancy and sex and pregnancy – 1622.
– –
2212. 113. Syngnathus floridae Syngnathus
-
Frequency role reversal. Molecular Molecular reversal. role – 858.
– 399. - Dependent Sexual Sexual Dependent Environmental
Revealed by by Revealed - role -
This article isThis article by protected copyright. All rightsreserved. notatus Apogon Accepted cardinalfish mouthbrooding the in fertilization timingof behaviorand Spawning (1983) Kuwamura T 233 Fishes,of 58, male. Biology mouthbrooding Environmental cardinalfish mouthbrooding paternal the cannibalism Filial in T (2000b) A, Taniuchi Kume G,Yamaguchi lineatus A, Ao Kume G,Yamaguchi 469 65, of Fishes, Biology Environmental vitellogenesis. without Oogenesis males: cannibalistic deceive to by cardinalfish female production Dummy(2002) egg I A, Aoki Kume G,Yamaguchi 63, 727 Behaviour, mouthbroo inapaternal output determines reproductive size Male Kolm N(2002) Sciences Biological B: Royal Society the of Proceedings fish. mouthbrooding males apaternal large in for eggs larger Females produce Kolm N(2001) Applied Ichthyology, of imberbis. Journal Apogon fish, Article cardinal Mediterranean the of parameters reproductive and growth Age, N(2007) NR, Raventos Klein http://www.montana.edu/kalinowski/Software/Mykiss.htm. Myki S (2009) Kalinowski 551 Resources, 10, Ecology data.Molecular genotype multilocus from inference sibship and program parentage for a COLONY: J(2010) OR,Wang Jones 461 10, Ecology, regimes.selection Molecular goby sand of populations two mating in patterns genetic rates and sneaking of similarity Surprising JC(2001) C, Avise Kvarnemo K, Lindstrom D, AG,Walker Jones sex the in quality Mate A,AviseJC(2000) G,Berglund AG,Rosenqvist Jones - role
in Tokyo Bay, Japan. Fisheries Science, 66, 947 Science,66, Bay, Japan. Fisheries Tokyo in - Apogon lineatus Apogon reversed pipefish reversed pipefish . Japanese Journal Journal . Japanese – 733.
ss ki I, Taniuchi T (2000a) Reproductive biology of the cardinalfish the of cardinalfish biology Reproductive (2000a) T Taniuchi I, ki : eg - software for analyzing reproductive success. reproductive analyzing for software Syngnathus typhle Syngnathus g production by the female as the nutrition source for the the sourcefor female nutrition by the the as production g of Ichthyology, 30, 30, 61 Ichthyology, of – 469. . Oikos, 90, 321 90, . Oikos,
– 55 23, 675 – , 268, 2229 , 268, – 5. 954. 71.
– – – 678. 236. 326. experiencing disparate sexual sexual disparate experiencing – 22
fl 34. uenc
es multiple maternity in esmaternity in multiple ding fish. Animal fish. ding Apogon Apogon – 472.
This article isThis article by protected copyright. All rightsreserved. in andotherchemicals oil clove of Comparative efficacy SK (1997) PL, Wilson Munday Accepted48, 1089 Evolution, Paternity. Extrapair isRelatedto Birds Plumage in of The Brightness Evolution TR (1994) Birkhead AP, Moller 17, 5036 Ecology, polyacanthus Acanthochromis Miller 1793 ex offspring brood and eggs males fertilize which species in pipefish ina cuckoldry testsfor and system mating genetic The Avise JC(2001) EE,AG, Jones McCoy 57, 1590 Biology, Site fide (2000) M Marnane 77, 261 Society, Cambridge Philosophical the reviewsof Biological fish. teleost cannibalism Filial in A(2002) Manica 2151 Sciences, 279, Biological B: Royal Society the of Proceedings ArticleClutton D, Lukas 293. 3, 283 Physiology, and Behaviour Marine barrierreef. island great atheron Gobiidae) (Osteichthyes: of behaviour the reproductive on observations Field (1976) Lassig B Goby Coral Size Nakashima Y,Y(1993) Yogo Kuwamura T, quinquelineatus mou and paternal Nightspawning (1987) Kuwamura T doederleini cardinalfishes, mouthbrooding three of behavior reproductive Socialand (1985) Kuwamura T
– - 1800. Sims VC, Gerlach G, Kingsford MJ, Atema J (2008) Dispersal in the spiny damselfish, spiny Dispersal the in (2008) Atema J MJ, Kingsford G, VC, Gerlach Sims , A. niger and A. notatus. A.notatus. and niger , A.
Paragobiodon echinocephalus Paragobiodon . Japanese Journal of Ichthyology, 33, 33, 431 Ichthyology, of Journal . Japanese – - 277. – Brock TH (2012) Cooperative breeding and Cooperative breeding THBrock (2012) – 1600. 5048.
lity and homing behaviour in coral reef cardinalfishes. Journal of Fishof Journal reefcardinalfishes. coral behaviour in andhoming lity – , a coral reef fish species without a larval pelagic stage. Molecular Molecular stage. pelagic alarval without species reeffish , acoral 1100.
Environmental . Ethology, 6 95, . Ethology, - assortative Monogamy and Paternal Egg Care in a Care in PaternalEgg and Monogamy assortative
Biology of Fishes, 13, 17 Fishes,13, of Biology thbrooding of the cardinalfish cardinalfish of the thbrooding – 434. 5 – 75.
monogamy in mammalian societies. mammalianmonogamy societies. in
– ternally. Molecular Ecology, 10, 10, Ecology, Molecular ternally. Paragobiodon spp Paragobiodon 215 6.
– 24.
Cheilodipterus Cheilodipterus . Apogon Apogon – This article isThis article by protected copyright. All rightsreserved. York. New Press, Academic models. to probability Introduction (1997) Ross SM Accepted 167 Fishes,of 92, Environmental Biology Butterflyfish. Tahitian JM ( Reavis RH,Copus 229 43, and Sociobiology, Ecology Behavioral monogamous? is the Why coral GW (1998) Reavis RH,Barlow 847 Genetics, 6, Nature reviews. solutions. Genotypi P (2005) A, Bellemain Taberlet E, Bonin F, Pompanon 70,1512 FishBiology, of Journal cardinalfish. semi Apparent (2007) RS, Takemura A Pisingan Parentalcare (1979) ZaretT MJ, Perrone 345 47, of Fishes, Biology Environmental Malawi. from fish Lake a cichlid zebra, Pseudotropheus in (1996) Polygynandry I A,Kornfield Parker cardina mouthbrooding paternal condition its and ornamentation Male Y(2003) Yanagisawa Fukumori N, K, Okuda Article cardinalfish costs The (2001) N Okuda 5 18, Ethology, Journal of (Pisces: Apogonidae). cardinalfishes sympatric two between behavior malecannibalistic in differences Interspecific (2000) N Okuda 273 58, Animal Behaviour, canniba male brood and strategy mating Female (1999) N Okuda 15, 327 Ecology, Behavioral sunfish. males bluegill in parasitic by sired offspring of performance Increased Neff BD(2004) of anaesthetization Apogon notatus Apogon Pomacentrus amb 2011) Monogamy in a feeding generalist, afeeding in 2011) Monogamy of reproduction to males and females of a paternal mouthbrooding mouthbrooding apaternal males females to of and reproduction of – . Journal of Fish Biology, 58, 776 58, Biology, of Fish . Journal 279. – 331. lfish with extraordinary sex roles. Journal of of Journal sex roles. withextraordinary lfish
oinensis
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This article isThis article by protected copyright. All rightsreserved. 38 wolves Ethiopian ( in avoidance inbreeding Sillero Sciences B:Biological Series London. of Society care topaternal Relating paternity BC (2002) Sheldon, 2531 defence.Molecular nest with biparental fish monogamous cichlid a of socially broods in ( S C, Koblmüller Sturmbauer K, Mattersdorfer Sefc KM, tits ( extra Effects and social of (2013) Kempenaers B E, Schlicht 4352 19, sparrows, song in status social and spatial location Genotype, assignment: paternity Comprehensive (2010) JM Reid T, Bucher ArceseP, LF, RJ,Keller Sardell 623 7, GeneticsResources, markers.Conservation microsatellite Pyjama cardinalfish the in relationships genealogical Resolving (2015) Berumen ML H, Mansour GP, HB, Jones Harrison T, Rueger 425 186, Oecologia, coral reefcardinalfish. f Site GP(2018) Jones NM, Gardiner T, Rueger 1585 27, Ecology, Behavioral acoralin reefcardinalfish. pairing assortative size leadsto matechoice male female and matters: Size GP(2016b) Jones NM, Gardiner T, Rueger of Journal live. to new place a find displaced everyone: for cardinalfish is not Homing GP(2016a) Jones NM, Gardiner T, Rueger 119 107, Processes, Behavioural cardinalfish. reef acoral in GP(201 Jones NM, Gardiner T, Rueger
Accepted, 331 Article Cyanistes caeruleus Cyanistes – 25 - Zubiri C, Gottelli D, Macdonald DW (1996) Male philopatry, extra Male philopatry, DW (1996) Macdonald D, Gottelli C, Zubiri – 43. – 340. 4364.
). Evolution, 67,1420 Evolution, ).
Fish Biology, 89, 2182 89, Biology, Fish , Sphaeramia nematoptera , Sphaeramia 4) Relationships between pair formation, site fidelity and sex fidelity site formation, pair between Relationships 4) – Canis simensis Canis 434. – 1434. idelity facilitates pair formation in aggregations of of aggregations in formation idelityfacilitates pair
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. Philosophical Transactions of the Royal Royal the of Transactions Philosophical 2008) High frequency of multiple paternity multiple paternity of frequency High 2008) ). Behavioral Ecology and Sociobiology, Sociobiology, and Ecology Behavioral ).
- – 350. - pair mating on sexual selection in blue blue in selection sexual on mating pair 26. Melos
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E cology, 17, 17, cology, - This article isThis article by protected copyright. All rightsreserved. differe Sex A,AhnesjiiI(2011) Berglund I, Ahnesjö A, Vincent Accepted fromapogonid of ecology Reproductive (2004) AV. Volpedo Vagelli AA, Neptune and Kong Hong of Colony Crown British Publications, inreeffishes.T.F.H. Reproduction (1984) RE Thresher sizecoral in social group PL,J VJ, Munday Thompson 109 21, Ecology, fish.Evolutionary mouthbrooding a paternal inmales of strategy aconditional as cannibalismFilial Yanagisawa N, Y(2007) Okuda Takeyama T, doed cannibalismby filial of pattern Seasonal Yanagisawa N, Y(2002) Okuda Takeyama T, 1405. 1392 Biology,26, Evolutionary of Journal awarbler. in sexualof selection strength the constrains Freeman Taff CC, Article 2865 Sciences, 274, extra fitness through females increase Reed bunting Meyer R, DR(2007) Feignoux KeiserM, SM, Suter 1725 61, Sociobiology, bicolor ( treeswallows Female RJ(2007) Robertson JT, Lifjeld MK,O, Kleven Stapleton Orlando. Press, Academic sys animalmating of evolution and the Sperm(1984) competition RL Smith 1323 BD),pp. Burks (ed Mexico, of America north in of Hymenoptera Catalog Family In: Formicidae. DR(1979) Smith erleini -
pair mating with genetically dissimilar males. Proceedings of the Royal Society B: Biological Biological B: Royal Society the of Proceedings males. dissimilar with matinggenetically pair ) increase offspring heterozygosity through extrapair mating. Behavioral Ecology and Ecology mating.extrapair Behavioral through heterozygosity ) increaseoffspring
mouthbrooding males. Journal of Fish Biology, 61, 61, 633 Biology, Fish of males. Journal mouthbrooding Indonesia - Gallant CR, Dunn CR, Dunn Gallant City, NJ.City, – 2871. – 1733. – -
with direct development. Environmental Biology of Fishes, 70, 235 Fishes,70, of Biology Environmental development. direct with dwelling fishes. Coral Reefs, 26, 165 26, Reefs, Coral fishes. dwelling 1467. Smithsonian Institution Press, Washington, DC. Press, Washington, Institution Smithsonian 1467.
ones GP (2007) Habitat patch size and mating system as determinants of of determinants mating as system Habitat sizeand patch GP(2007) ones
PO, Whittingham LA (2013) Spatial distribution of of nests distribution Spatial PO, Whittingham(2013) LA Pterapogon kauderni Pterapogon –
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This article isThis article by protected copyright. All rightsreserved. Accepted a in hypotheses multiple testsof polygyny: for ispotential there when Monogamy JonesGP(2008) PM, PL, Buston Munday MYL, Wong Anim society. a hermaphroditic C, Plan Fauvelot MYL, Wong 150. a in Coral Change Sex and Monogamy Size, Facultative Patch Habitat PL, GP(2005) Jones Munday MYL, Wong Revie Annual Evidence. and Monogamy:Hypotheses of TheEvolution RL (1980) Tilson J, Wittenberger Article Press. University Harvard NewSynthesis. The Sociobiology: EO (1975) Wilson Mate ambiguousconcept. an Monogamy: U(1983) Seibt W, Wickler 66, 281 Behaviour, Animal netbenefit? or constraints ecological cleaning goby inthe monogamy Social (2003) IM Côté Whiteman EA, 79, 351 Society, Philosophical ( IM Côte Whiteman EA, 877 35, Animal Behaviour, Extra (1987) Westneat DF 34, 435 Ecology, Behavioral population. ina pipefish behavioural
w of Ecology and Systematics, 11, 197 Systematics,11, and Ecology w of - dwelling Fish dwelling 2004) Monogamy in marine fishes. Biological reviews of the Cambridge the of reviews Biological fishes. marine Monogamy in 2004) - – evidence. genetic bird: monogamous apredominantly in fertilizations pair 886. es S, Buston PM (2012) Discrete and continuous reproductive tactics reproductive in continuous and Discrete (2012) PM Buston es S, – al 75. , Caracanthus unipinna , Caracanthus
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– This article isThis article by protected copyright. All rightsreserved. Accepted Article
This article isThis article by protected copyright. All rightsreserved. Accepted Article