Table Of ContentCommunicative&IntegrativeBiology5:3,272–274;May/June2012;G2012LandesBioscience
Evolutionary developmental biology in cycad phenology
Root Gorelick1,* and Thomas E. Marler2
1DepartmentofBiology;CarletonUniversity;Ottawa,ONCanada;2WesternPacificTropicalResearchCenter;UniversityofGuam;Mangilao,GuamUSA
Werecentlydescribedlackofpheno- and evolution describes processes among
typic plasticity in reproductive generations.Inwritingaboutfossilcycads,
organ development and substantial plas- Mamay4 first suggested that angiosperm
ticityinvegetativeorgandevelopmentfor carpels evolved from megasporophylls,
the cycad Cycas micronesica. Is there an possiblyofcycads.Inmoremodernterms,
evo-devo explanation for the disparity in examining regulatory genes, Frohlich5
© 2012 Laphenontypicdplasticeity osf veg etaBtive vis. osuggessted tchat aingieospermncarpecls evoelved .
reproductive organs? Despite modularity, from microsporophylls. These two hypo-
might evolution of cycad phenology be theses are probably incommensurate
controlled more by drift than selection? given that female and male strobili of
cycads are homologous, unlike strobili of
all other extant gymnosperms.6 Cycad
Introduction megastrobili and microstrobili are effec-
Do not distribute.
tively a telescoped flush of leaves (Fig.1).
Understandingthedevelopmentalpatterns Both female and male strobili are still
of vegetative and reproductive organs highly modified, so we still expect
and factors that influence those patterns differentdevelopmentalpathwaysinveget-
is of critical importance for conserving ative leaves, megastrobili and micro-
rare plants. We recently determined that strobili. Development in cycads is
leaf and leaflet expansion of the endan- undoubtedly modular, as in other gym-
gered Cycas micronesica were influenced nosperms,7 although maybe not as modu-
by spatial and temporalfactors, but repro- lar as in angiosperms.8 Thus ontogeny of
ductiveorganexpansionwasunaffected or various cycad organs should progress
only minimally influenced by the same differently from other organs in the same
factors.1 We pointed out that empirical individual plant.
approaches for fitting models to organ We expect different developmental
growth and development may be used to timing in vegetative vs. reproductive
inform horticultural or conservation ques- organs because cycad strobili are likely
tions of other rare cycad taxa. Here we highlyendoploid.Mostmalecycadstrobili
argue that this approach may improve our are thermogenic.9-12 Thermogenesis prob-
Keywords: Cycadaceae, Cycadales, understanding of the evolutionary and ably requires extra mitochondria, as we
endoploidy, ontogeny, organ developmental biology of cycads. see in several skunk cabbage (Symplo-
development, phenology carpus) species.13,14 While almost exclu-
Modularity and Endoploidy sively documented in angiosperms, plants
Submitted: 01/19/12
in Cycads have plenty of endoploidy, especially
Accepted: 01/20/12
succulent plants,15 which might include
http://dx.doi.org/10.4161/cib.19428 While slow to gain traction in botany, stems and strobilus axes in cycads.
*Correspondenceto:RootGorelick; especially in studies of gymnosperms (but Furthermore, animal tissues with high
Email:[email protected] see refs. 2 and 3), evo-devo has become metabolic demand are often highly endo-
oneofthemostpromisingandproductive ploid, such as heart muscles, flight
Addendumto:MarlerTE,DongolN.Modelsto perspectivesinbiology.Thisshouldnotbe muscles and liver cells.16 We suspect that
describeCycasmicronesicaleafandstrobili surprising given that development endoploidy provides a way around other-
development.HortScience2011;46:1333–7.
describes processes within a generation wise rate-limiting production of mRNA.
272 Communicative&IntegrativeBiology Volume5Issue3
ARTICLEADDENDUM
Efforts to confirm endoploidy in cycad
strobili are warranted because endoploidy
alters developmental rates insofar as
mitotic cycle rates are inversely propor-
tional to ploidy levels17 and probably
inversely proportional to chromosomal
content per nucleus, i.e., C-values.
Environment and Cycad Evolution
There are four modes of evolutionary
response to changing environments: (1)
environmental tracking, (2) phenotypic
plasticity, (3) bet hedging, and (4) extinc-
tion.18Apriori,weexpectgreaterenviron-
mental tracking and phenotypic plasticity
in vegetative structures because the indi-
vidual plant cannot grow without leaves.
However, we expect more bet hedging
©(risk ave2rsion)0in r1eprodu2ctive orgLan andes Bioscience.
productionforanyperennialplant;especi-
ally in Cycas micronesica, which makes
large investments in both female and
male strobili.19 But these are all mechan-
isms by which organisms evolve via selec-
tion. By contrast, Gorelick and Olson20
Do not distribute.
argued that drift should play a dispropor-
tionate role in cycad evolution compared
with selection because of the peculiar
genomic architecture and small popula- Figure1.ACycasseemanniimegastrobilus(or‘indeterminatestrobilus’sensuinref.28)emergesas
aflushofmegasporophyllsbearingnakedovules,whicharealmostcertainlyhomologous
tion sizes (see also ref. 21). Similarly,
tothepinnatelycompoundvegetativeleaves.ThegenusCycascontainsomespecieswithpinnately
Lynch and Conery22 hypothesized that compoundmegasporophylls,e.g.,C.revolutaandC.pectinata,11whileallmembersofthegenushave
large genome size, which we see in newflushesofvegetativeleavesthatemergefromthecenterofthemegastrobilus,asseen
cycads,20,23 may be maladaptive. Thus inthisfigure,furtherindicatinghomologybetweensporophyllsandvegetativeleavesincycads.
developmental rates of different plant
parts may be nothing more that what
Gould and Lewontin24 mistakenly called trajectories of cycads may be a pre- extant gymnosperms,6 the relative roles
spandrels. Maybe there are no adaptation- requisite for restoring habitats during of selection and drift may not be the
ist explanations nor fitness benefits to the recovery efforts. Thus far, we have only same in evolution of cycads vs. other
developmentalpatternswedescribed.1Or, examined phenology and evolutionary gymnosperms. Given that cycads are the
alternatively, maybe these developmental responses in the most basal genus of most basal of living seed plants, it is
patternsarenothingmorethanacorollary cycads, Cycas, with its disaggregated incumbent upon us to better understand
of endoploidy levels, which we presume female strobili. Do Zamiaceae also show these fascinating plants. Measurement of
are greater in thermogenic cones than in lack of phenotypic plasticity in cone effective population sizes, plasticity, het-
other plant parts. development? Because of the putative erochrony, and endoploidy will help
recent ancestry of all extant cycads,27 we immensely in answering these evolution-
Conclusions anticipate similarities among all living ary questions about cycads and may well
cycads, which may not be due to any help in their conservation.
Cycads are a threatened group of plants selective advantage. Does plasticity of
worldwide25forwhichrecoveryplanshave cycad male cone development differ Acknowledgments
already been proposed or implemented from that of other gymnosperms? RootGorelickthankstheNaturalSciences
forsometaxa(e.g.,seeref.26).Afullunder- Because cycad male cones are presumably and Engineering Research Council of
standing of evolutionary developmental not homologous with those of other Canada (NSERC) for financial support.
www.landesbioscience.com Communicative&IntegrativeBiology 273
References 11. Norstog KJ, Nicholls TJ. The biology of cycads. 19. Marler TE.Cycad mutualist offers morethan pollen
CornellUniversityPress,Ithaca.1997. transport. Am J Bot 2010; 97:841-5; PMID:
1. Marler TE, Dongol N. Models to describe Cycas 12. Terry I, Moore CJ, Walter GH,ForsterPI, Roemer 21622449;http://dx.doi.org/10.3732/ajb.0900251
micronesicaleafandstrobilidevelopment.HortScience
RB,DonaldsonJD,etal.Associationofconethermo- 20. Gorelick R, Olson K. Is lack of cycad (Cycadales)
2011;46:1333-7.
genesis and volatiles with pollinator specificity in diversityaresultofalackofpolyploidy?BotJLinnSoc
2. AbercrombieJM,O’MearaBC,MoffattAR,Williams Macrozamia cycads. Plant Syst Evol 2004; 243:233- 2011; 165:156-67; http://dx.doi.org/10.1111/j.1095-
JH.Developmentalevolutionoffloweringplantpollen 47;http://dx.doi.org/10.1007/s00606-003-0087-x 8339.2010.01103.x
tubecellwalls:callosesynthase(CalS)geneexpression
13. Knutson RM. Heat production and temperature 21. Gorelick R. Evolution of cacti is largely driven by
patterns. EvoDevo 2011; 2:14; PMID:21722365;
regulation in eastern skunk cabbage. Science 1974; geneticdrift,notselection.Bradleya2009;27:41-52.
http://dx.doi.org/10.1186/2041-9139-2-14
186:746-7;PMID:4417289;http://dx.doi.org/10.1126/ 22. Lynch M, Conery JS. The origins of genome com-
3. FrohlichMW.MADSaboutGnetales.ProcNatlAcad science.186.4165.746 plexity.Science2003;302:1401-4;PMID:14631042;
SciUSA1999;96:8811-3;PMID:10430847;http://
14. Ito-InabaY,HidaY,InabaT.Whatiscriticalforplant http://dx.doi.org/10.1126/science.1089370
dx.doi.org/10.1073/pnas.96.16.8811
thermogenesis? Differences in mitochondrial activity 23. Zonneveld BJM. Genome sizes for all genera of
4. MamaySH.Paleozoicoriginofcycads.USGeolSurv andproteinexpressionbetweenthermogenicandnon- Cycadales. Plant Biol 2012; 14:253-6; PMID:
ProfPap1976;934:1-48. thermogenic skunk cabbages. Planta 2009; 231: 22117644
5. FrohlichMW.Anevolutionaryscenariofortheorigin 121-30;PMID:19859730;http://dx.doi.org/10.1007/ 24. Gould SJ, Lewontin RC. Spandrels of San Marco
of flowers. Nat Rev Genet 2003; 4:559-66; PMID: s00425-009-1034-z and the Panglosian paradigm: a critique of the
12838347;http://dx.doi.org/10.1038/nrg1114 15. DeRocherEJ,HarkinsKR,GalbraithDW,Bohnert adaptationist program. Proc RSoc Lond SerB, Biol
6. Mundry M, Stutzel T. Morphogenesis of male HJ.Developmentallyregulatedsystemicendopolyploid Sci1979;205:581-98;http://dx.doi.org/10.1098/rspb.
sporangiophoresofZamiaamblyphyllidiaD.W.Stev. in succulents with small genomes. Science 1990; 1979.0086
Plant Biol 2003; 5:297-310; http://dx.doi.org/10. 250:99-101; PMID:17808240; http://dx.doi.org/10. 25. HoffmannM,Hilton-TaylorC,AnguloA,BöhmM,
1055/s-2003-40791 1126/science.250.4977.99 Brooks TM, Butchart SH, et al. The impact of
7. Vázquez-Lobo A, Carlsbecker A, Vergara-Silva F, 16. Anatskaya OV, Vinogradov AE. Heart and liver as conservation on the status of the world’s vertebrates.
Alvarez-Buylla ER, Piñero D, Engström P. Charac- developmentalbottlenecksofmammaldesign:evidence Science 2010; 330:1503-9; PMID:20978281; http://
terization of the expression patterns of LEAFY/ fromcellpolyploidization.BiolJLinnSocLond2004; dx.doi.org/10.1126/science.1194442
FLORICAULA and NEEDLY orthologs in female 83:175-86; http://dx.doi.org/10.1111/j.1095-8312. 26. Forster PI. Recovery plans for endangered cycads: a
©aanndd mTaa2lxeucs:oniemspol0fictahtieocnosniff1oerrgceunrreerna2tPiecveoa,-dPeovd oochaLryppuos-, a17. 2L0ene04H.0O03,7D7da.xvidsonJeM,DurosnioRJ. EndBoreplicatioin: omosfoCdeyclassetmcoegfaocabrjepicatifvreoesmanQduaecentnioslnasndu,siAncgustthraelieaex.aMmepmle .
theses for gymnosperms. Evol Dev 2007; 9:446-59; polyploidywithpurpose.GenesDev2009;23:2461- NYBotGard2007;97:3-31.
PMID:17845516; http://dx.doi.org/10.1111/j.1525- 77; PMID:19884253; http://dx.doi.org/10.1101/gad. 27. NagalingumNS,MarshallCR,QuentalTB,RaiHS,
142X.2007.00182.x 1829209 Little DP,MathewsS.Recent synchronous radiation
8. WilliamsJH.Novelties ofthefloweringplantpollen 18. Simons AM. Modes of response to environmental of a living fossil. Science 2011; 334:796-9; PMID:
tubeunderliediversificationofakeylifehistorystage. change and the elusive empirical evidence for bet 22021670;http://dx.doi.org/10.1126/science.1209926
Proc Natl Acad Sci U S A 2008; 105:11259-63; hedging. Proc R Soc Lond Ser B, Biol Sci 2011; 28. Stevenson DW. Morphology and systematics of the
PMID:18678915; http://dx.doi.org/10.1073/pnas. 278:1601-9; PMID:21411456; http://dx.doi.org/10. Cycadales.MemNYBotGard1990;57:8-55.
0800036105 Do no109t8/rsp b.20d11.0176istribute.
9. Tang W. Heat production in cycad cones. Bot Gaz
1987;148:165-74;http://dx.doi.org/10.1086/337644
10. TangW.Heatandodourproductionincycadcones
andtheirroleininsectpollination.In:StevensonDW,
NorstogKJ,eds.Thebiology,structure,andsystema-
tics of the Cycadales. Proceedings of Cycad 90, the
secondinternationalconferenceoncycadbiology.Palm
&CycadSocietiesofAustralia,Milton,1993:140-7.
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