Sexual Modes in the Colonial Kamptozoan Genus Barentsia

8 Pages·1997·3.8 MB·English

by  K Wasson

Reference:Bwl.Bull. 193: 163-170.(October, 1997)
Sexual Modes in the Colonial Kamptozoan
Genus Barentsia
KERSTIN WASSON
DepartmentofBiology, University ofCalifornia, Santa Cm:,, California 95064
Abstract. Sexualmodeincolonialanimalsisexpressed therecanbe multiplecoloniespergenet(geneticindivid-
at the zooid, colony, and genet level; all three must be ual: all tissue derived mitotically from one zygote) pro-
characterized to understand sexuality in these animals. I ducedearlyindevelopmentbypolyembryony,orlaterby
carried out such an examination ofthe sexual modeofa fragmentation orencapsulation. Such animals have three
colonial kamptozoan (entoproct). Barentsia hildegardae, levels of organization: the zooid, the colony, and the
at Friday Harbor. Washington. Calyces never contained wholemulticolonygenet.Onewayofclassifyingthesex-
bothovariesandtestes,andcoloniesnevercontainedboth ual modes of colonial animals (Wasson and Newberry,
maleandfemalecalyces.Calycesandcolonies(including 1997) is to designate each of the three organizational
replicate colonies from the same genet) monitored over levelsasgonochoric(G).sequentiallyhermaphroditic(S).
two years did notchange sex. Theseresults suggest that orsimultaneously hermaphroditic (H). According to this
B. hildegardae iscomprehensivelygonochoric. Forcom- system, 10 modes ofcolonial sex are possible (Fig. 1),
parison, Iexaminedthesexualmodeoffiveotherspecies although only 5 have known examples among animals
in the genus Barentsia. Barentsia benedeni, B. conferta, (Wasson and Newberry, 1997).
and B. ramosa also appearto be comprehensively gono- Few researchers investigating colonial animals have
choric.Barentsiadiscrete!ishermaphroditicatthecolony thoroughlyexaminedthesexualmodeofzooids,colonies,
level,withgonochoriccalyceswhosesexisenvironmen- and whole genets ofa single species. Many report only
tallydetermined,asnotedbypreviousworkers.Barentsia thesexual modeofthe zooids,leavinguncertain thesex-
aggregata has simultaneously hermaphroditic calyces; ual mode ofthe colony or the whole genet. We cannot
this was reported by the authors who described it. but examine the ecology and evolution ofmating systems in
hasescaped notice in subsequent reviewsofkamptozoan colonial animals if words such as gonochoric and her-
biology. There are thus three contrasting modes of sex maphroditic are used without specifying the level to
within the genus Barentsia. All three modes also occur which they apply. Furthermore, colonial animals have
in colonial cnidarians, and two of them are known in rarely been monitored over time, so it has been difficult
bryozoans, colonial hemichordates. and colonial uro- to distinguish gonochorism from sequential hermaphro-
chordates. These disparate sexual modes may have ditism (hermaphroditism with discrete, separated periods
evolved as adaptations todiffering environmental condi- ofmale and female maturity) at any level.
tions orpopulation densities. Thepurposeofthisinvestigationwastodescribethor-
oughly the sexual mode of one barentsiid kamptozoan
Introduction (entoproct), Barentsia hildegardae, by examining all
threelevelsofcolonialorganizationandmonitoringthem
Colonial animals display a diversity ofsexual modes. overtime. Barentsiidsare small marine suspension feed-
Every colonial species can be examined at two levels, ers; barentsiid colonies superficially resemble those of
that ofthe zooid (the structure that is iterated to form a hydroids. Cuplike calyces containing U-shaped guts and
colony) and thatofthecolony. In manycolonial species, ringedbytentaclesareborneon stalksarisingfrompros-
trate stolons. The calyx is the sexually reproductive unit
ofabarentsiidkamptozoanzooid,atsexualmaturitycon-
Received5February 1997;accepted5May 1997. tainingtestes,ovaries,orboth. Althoughthekamptozoan
163
164 K. WASSON
GENET
SEXUAL MODES IN THE GENUS BARENTSIA 165
Otherbarentsiidspecies Results
BarentsiaconfertaWasson. 1997,andB. ramosa(Rob- Barentsia hildegardae
ertson, 1900)arebothendemictothenortheasternPacific; Every sexually maturecalyx ofBarentsia hildegardae
bothofthesespeciesarefoundprimarily inthelowinter- was either male (Fig. 2a) or female (Fig. 2b); a calyx
tidal zone of exposed coasts (Wasson, 1997). Between nevercontainedbothtestesandovaries.Furthermore,ex-
May 1991 andJuly 1995, I collected colonies ofB. con- amination of thousands of calyces during the course of
ferta fromarocky shelfandB. ramosa fromunderover- this study (in field samples and in slide-grown colonies)
hangs in the low intertidal zone at Natural Bridges State neverrevealedacalyxwithripeovariesanddegenerating
Beach. Santa Cruz. California. B. conferta grew mainly testes. or vice versa.
in dense aggregations on articulated coralline algae; B. Most 2-cnr plots on ascidians at Friday Harbor con-
ramosa grew in denseclumps on rocky overhangs. Iex- tained calyces mainly or entirely of one sex (Fig. 3a).
aminedatotalof48 aggregations(presumedcolonies)of although many plots contained calyces of both sexes. I
B. conferta and 33 aggregations ofB. ramosa, counting was unable todetermine how manycolonies were grow-
male, female, and immature calyces. inginasingleplot.Inplotscontainingbothsexes,Inever
Barentsia benedeni (Foettinger, 1887) is acosmopoli- observed male and female calyces growing along the
tan species, found in bays and harbors around the world same stolon.
(Wasson, 1997). In July 1993, I collected five mussels Single colonies grown on slides always consisted of
bearing colonies of B. benedeni from floating docks in calycesofonlyonesex.Ofthe200slidecoloniessampled
Lake Merritt, Oakland. California. The calyces in these eight times over one year, none was ever found with a
colonies were not sexually mature. I removed 30 small mix ofsexes. Furthermore, none ofthe 200 slide-grown
colony portions from the mussels and grew these frag- colonies changed sex over the year (June 1993-July
mentsonglassslidesonaseatableatLongMarineLabo- 1994) ofmonitoring. Although most ofthe 200 colonies
ratory, Santa Cruz. California. In February 1994. when were either dead or nearly so by the end of the second
21 ofthese30coloniessexuallymatured.Iexaminedand year. 31 colonies were sexually mature in August 1995.
sexedallthecalycesofeachcolony. I alsoexaminedand Allofthesewerestillthesamesexastheoriginalcolony
sexedapreservedcolonyofthis speciesfrom Lake Mer- had been.
ritt. in the collection ofthe California Academy of Sci- Over the yearlong sampling period, all 70 replicate
ences (#10510). colonies of seven genets remained the same sex as the
Barentsia discreta (Busk. 1886) is widely distributed originalcoloniestheyweretakenfrom,regardlessofsize
in most ofthe world's oceans, in bothdeep and shallow or age. and regardless of whether they were raised in
waters (Wasson, 1997). In October 1994 I obtained two boxeswithcoloniesofthesameoroppositesex. Further-
large colonies of B. discreta from Mission Bay. San more. 17replicatecoloniesrepresentingfourgenetswere
Diego.California.Thecalyceswere not sexually mature. still sexually mature at the end of the second year; all
I removed 1 small portionsofonecolony and 11 ofthe were still the same sex as their source colonies.
otherandgrewthemonglassslidesonaseatableatLong Colonies grown on glass slides and kept in jars of
Marine Laboratory. In August 1995, when the calyces seawaterinthelaboratoryundervariousfood,waterflow,
had sexually matured. I examined these 21 slide-grown and temperature levels (as part of growth experiments
colonies forthepresence ofmale, female, and immature unrelated to the present study) also contained calyces of
calyces. I also examined specimens of6. discreta in the only asinglesex.anddidnotchangesexoverthecourse
collection ofthe Allan Hancock Foundation, University ofthe three-month experiments.
of Southern California. This material (57D/1-10) con-
sistedof 10wholemounts (slides)ofcoloniesfromCali- Barentsia conferta, B. ramosa, andB. benedeni
fornia. Mexico. Ecuador, and Peru.
Barentsia aggregate! Johnston and Angel, 1940, is a Calyces of Barentsia conferta and B. ramosa always
little-known species of Antarctic waters. I examined all contained either testes or ovaries, never both. Aggrega-
the specimens of B. aggregata deposited in the South tionsofcalycesofthesespeciesalwaysconsistedmainly
Australian Museum, Adelaide, by Johnston and Angel orentirely ofone sex (Fig. 3b, 3c). In aggregations that
fromcollectionsoftheBANZAntarcticResearchExpedi- contained both sexes, male and female calyces were not
tion (1929-1931) at Macquarie and Heard Islands. This randomly distributed. Instead, the aggregation consisted
material(E944-946;948-953;2132.2133.andunregis- mostlyofcalycesofonesex,andthecalycesoftheoppo-
teredspecimensintheBANZAREcollection)consistsof site sex were limited to one patch or one region of the
10 preserved (wet) colonies, 9 whole mounts (slides) of aggregation.WheneverIfoundanaggregationcontaining
colonies, and 31 slides ofsectionedcalyces. both sexes. I teased it apart and found that the male and
166 K. WASSON
a femalecalycesweregrowingondifferentstolons; Inever
observed male and female calyces growing on the same
stolon.
CalycesofBarentsiabenedenicontainedeitherovaries
ortestes.neverboth.Eachofthe21 slide-growncolonies
from Lake Merritt consisted ofcalyces of a single sex,
although colonies did not contain very many sexually
mature calyces (Fig. 3d). There were considerably more
female than male colonies, probably because I had
oversampledasinglelargefemalecolonywhenoriginally
removing colony portions from the mussels to generate
the slide-grown colonies. The colony at the California
Academy of Sciences (#105010) was huge and over-
whelmingly female, consisting ofabout 950 female and
85 immaturecalyces(nomalecalyceswerepresent);this
colony is represented by the leftmost bar in Figure 3d.
Barentsia discrete
CalycesofBarentsiadiscreta(bothmuseumandslide-
grown colonies) containedeithertestes orovaries, never
100pm both. In June 1995, when the slide-grown colonies first
became sexually mature,onlymale(andimmature)caly-
ceswerepresent.InJuly 1995.afewfemalecalyceswere
b presenttogetherwithnumerousmalecalycesinthesame
colonies. InAugust 1995. 11 ofthe21 slide-growncolo-
niescontained both male andfemalecalyces atthe same
time, while 10containedonly male calyces; nocolonies
consistedonly offemale calyces (Fig. 3d). Fivecolonies
in the collectionofthe Allan HancockFoundation (57D/
1,3,7,8, 10)fromCalifornia.Mexico,Ecuador,andPeru
also had male and female calyces arising from the same
stolon within acolony.
Barentsia aggregata
Many calyces in the South Australian Museum's col-
lection of Barentsia aggregata from the Antarctic con-
tainedbothovariesandtestes.Sectionedmaterial(E2132)
revealedparticularlyclearlythesimultaneouspresencein
a single calyx of testes with ripe sperm, ovaries with
yolkyeggs,andabroodchamberwithembryos.Although
most preserved colonies consisted ofcalyces containing
both ovaries and testes, a few contained only male or
only female calyces.
Discussion
M Comprehensive gonochorism (mode GgG):
I
common in the genus Barentsia?
Figure2. Barentsiahildegardae.(a)Malecalyxinright-sideview;
nghttestismarkedbyarrow,(b)Femalecalyxinright-sideview;right Ofall the potential sexual modes forcolonial animals
ovarymarkedbysmallerleftarrow;broodchambercontainingembryos (Fig. 1). mode GgG is the most difficult to demonstrate.
markedbylargerrightarrow.Scalebarappliestobothaandb. To eliminate the possibility ofsequential hermaphrodit-
ism at any level, zooids. colonies, and genets must be
monitored over time. To thoroughly exclude genet her-
SEXUAL MODES IN THE GENUS BARENTSIA 167
Barenlsiahildegardae maphroditism, replicate colonies ofthe same genet must
also be examined.
The data forBarentsia hildegardae represent the first
compellingdemonstrationofcolonyandgenetgonochor-
a) ism(modeGgG)inakamptozoan. Earlierreportsofcol-
onygonochorisminthegenus(Table I)werelessreliable
because,basedasthey wereon isolatedorbriefobserva-
lln. tions of living colonies or scrutiny of fixed specimens,
theycouldnoteliminatethepossibilityofsequentialher-
Barentsiaconferta maphroditism at any level. These studies also did not
attempt to assess the sexual mode ofwhole genets.
Barentsia hildegardae evidently displays mode GgG.
Calyces contained gonads ofonly one sex, and did not
b) change sexovertime in slide-grown colonies. Every one
ofthe200slide-growncoloniescontainedcalycesofonly
one sex; none changed sex over the one-year sampling
period; those that survived through a second year re-
mained the same sex as well. Male or female, the 70
Barentsiaramosa replicate colonies of 7 genets also did not change sex
overthe entire sampling period.
Although slide-grown colonies ofB. hildegardae pro-
vided unambiguous evidence for comprehensive gono-
c) chorism, the samples of colonies growing on ascidians
(Fig. 3a) did not. Most ofthe 2-cnr plots were skewed
heavily toward male or female calyces, but many con-
tained a mix of sexes. I conclude that these ascidians
Barentsiabenedeni hostedmultiplecoloniesofB. hildegardaegrowinginter-
n n twined: each 2-cnr plot probably contained calyces
mainly from one colony (and thus ofone sex), but also
contained a few calyces from adjacent colonies (some-
d) times ofthe opposite sex). This result highlights the im-
portanceofknowingcolonyboundaries;inthiscase,field
sampling alone could not have distinguished mode GgG
III,,,,.. from mode HhG.
The more limited data for Barentsia conferta, B. ra-
Barentsiadiscreta mosa, andB. benedenisuggestthatthese speciesarealso
comprehensively gonochoric (mode GgG). Field sam-
pling was more strongly suggestive ofcolony gonochor-
ismforB. conferta(Fig.3b)andB. ramosa(Fig. 3c)than
e) for B. hildegardae (Fig. 3a). Both B. conferta and B.
ramosagrowmoredenselythandoesB.hildegardae,thus
limitingthepotentialforintrusionbycoloniesofdifferent
genets. The 21 slide-grown colonies ofB. benedeni had
fewsexuallymaturecalyces,butthepattern(Fig.3d)was
consistent with colony gonochorism, as was the huge,
female wholly female preserved colony that I examined. At the
Figure3. Patternsofsexdistributioninfivebarentsiidkamptozoan
species.Foreachspecies,allcalycesfromaplot,aggregation,orslide averageof127calyces,(c)Barentsiaramosa.Resultsfrom33aggrega-
weresexed microscopically. Percentmaturityisshownonthev-axis; tionsonrockyoverhangs;anaggregationcontainedanaverageof269
plots, aggregations, or slides are shown on the.v-axis andhave been calyces,(dlBarentsiabenedeni. Resultsfrom21 slide-growncolonies
arrangedbydecreasingfemalematurity andincreasingmalematurity, andonelargepreservedcolony(representedby left-mostbar);aslide
(a)Barentsiahildegardae. Resultsfrom40(2cm")plotsonascidians; containedanaverageof46zooids;thepreservedcolonycontained1035
aplotcontainedanaverageof38calyces,(b)Barentsiaconferta.Results calyces, (e)Barentsiadiscreta. Resultsfrom21 slide-growncolonies;
from48aggregationsoncorallinealgae;anaggregationcontainedan aslidecontainedanaverageof30calyces.
168 K. WASSON
TableI
SexualmodesreportedinthegenusBarentsia
Sexualmode Species
SEXUAL MODES IN THE GENUS BARENTSIA 169
nies overtime, although that is certainly the best way to outcrossing may be favored under stable environmental
observethetimingofmaturationandtodetecttendencies conditions and high population densities, where a mate
toward protandry orprotogyny. ofthe opposite sex is always likely to be nearby. Mode
It has been suggested that all Barentsia species have HhG. as in B. discrete, may combine some advantages
gonochoric calyces (Mariscal, 1975: Emschermann, of gonochorism (e.g., construction of more specialized
1994).JohnstonandAngel(1940).however,reportedher- reproductive structures) at the level of the calyx with
maphroditic calycesofBarentsiaaggregate!, and myex- someadvantagesofsimultaneous hermaphroditism (e.g..
amination oftheir material confirms that calyces ofthis doubling thechance ofencountering amate) atthe level
species often contain both mature testes and ovaries. ofthe genet (Ghiselin, 1969). Furthermore, a strategy of
Mode HhH thus is represented in the genus Barentsia phenotypic sex determination of calyces (as in B. dis-
(Table I). creta'sHhG)maybeadvantageousinunpredictableenvi-
Althoughmanycalycesweresimultaneouslyhermaph- ronments (Charnov and Bull. 1977) and under variable
roditic,justifying thedesignation ofthe species as HliH. populationdensities.Forexample,acolonymightcontin-
some calyces appeared to be only male or only female. ually adjustitsproductionofmale andfemalecalyces in
Perhapsaperiodofmalematurity precedes simultaneous responsetoenvironmentalcues, including local densities
hermaphroditism,andaperiodoffemalematurityfollows ofmale andfemalecalyces in neighboringcolonies. The
degeneration ofthe testes. Or, intriguingly. perhaps sex calyxhermaphroditism(HhH)oftheAntarcticB.aggreg-
determinationissolabile inthisspeciesthatfully mature atemaybefavoredunderstringentenvironmentalcondi-
calycescanbeeithermale,female,orhermaphroditic.To tions in which the overall chance offertilization is very
distinguishamongthesealternatives,livingcoloniesmust lowbecause thebreedingperiodisshort,growth isslow,
be observed overtime. andpopulationdensities are low. Undersuchconditions,
Harmer (1915) reported hermaphroditic calyces in a whengametesoftheoppositesexareonlyrarelyencoun-
kamptozoanfromIndonesiathatheidentifiedasBarentsia tered, calyx hermaphroditism may be a good strategy
laxa (but that almostcertainly represents an undescribed (Ghiselin. 1969). And simultaneous hermaphroditism
species, with tall, flexible, deeply annuluted rods). His mayalsoallow forself-fertilization,ifthebenefitsofany
illustration(pi.2,fig. 11 in Harmer. 1915)ofahermaph- sexatalloutweighthecostsofinbreeding. Ataxon such
roditic calyx is unconvincing; it appears to be a female as the genus Barentsia, in which closely related species
withembryos. His material (British Natural History Mu- have remarkably different sexual modes, would be an
seum 1916.8.23.38) is in such poor condition that I was excellentmodelsystemfortestingsuchhypothesesabout
not able to see ovaries and testes, so his report remains theevolutionofdifferentcolonial modesofsex,by map-
unconfirmed. pingecologicaldataaboutenvironmentalconditions,pop-
ulationdensity,andself-fertilizationonarobustphyloge-
A diversityofsexualmodes in thegenus Barentsia netic tree.
Thesuggestionthatmostorallspeciesofkamptozoans Comparisons with othercolonialanimals
arehermaphroditic (Nielsen, 1989)has been perpetuated
inmany invertebratezoologytextbooks(e.g.. Bruscaand Colonial cnidarians (hydrozoans and anthozoans) ex-
Brusca, 1990; Ruppert and Barnes, 1994). Within the press all three sexual modes (GgG. HhG. and HhH) that
genus Barentsia. hermaphroditic colonies with gono- barentsiid kamptozoans do (Fadlallah, 1983; Fautin,
choriccalyces(HhG)wereconsideredtherule(Emscher- 1992). In addition, somecolonial hydrozoans and antho-
mann 1985, 1994).However,thedatapresentedheredem- zoanshavemodeHhS,inwhichsequentiallyhermaphro-
onstrate that three sexual modes (GgG, HhG, and HhH) diticcalycesarenotsynchronized intheirsexchange, so
are expressed by species ofBarentsia, and that compre- that the colony as awhole is simultaneously hermaphro-
hensive gonochorism (mode GgG) may be at least as ditic (Wasson and Newberry. 1997). This mode has not
common as HhG. In fact, I hypothesize, on the basis yet been reported for a barentsiid kamptozoan.
ofarecent phylogenetic analysis ofnortheastern Pacific Bryozoans and colonial hemichordates (pterobranchs)
Barentsia species (Wasson, 1997), that comprehensive displaytwoofthethreemodes(HhG,HhH)describedfor
gonochorism is plesiomorphic for the genus, and her- barentsiidkamptozoans,butapparentlyhavenomembers
maphroditism is derived. with comprehensively gonochoric (GgG) colonies (Had-
Whatselectivepressuresmighthavefosteredtheevolu- field, 1975; Reed, 1991). Somebryozoans, likesomeco-
tion or maintenance of such contrasting modes of sex? lonial cnidarians, also exhibit mode HhS.
Comprehensive gonochorism(GgG), as inBarentsiahil- Colonialurochordates(ascidiansandthaliaceans)over-
degardae, prevents the self-fertilization that might occur whelmingly display one mode of sex also found in ba-
ifcalyces orcolonies were hermaphroditic. Such forced rentsiid kamptozoans, namely HhH (Berrill, 1975). A
170 K. WASSON
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