Plant Mating Systems

The remark­able diversity of mat­ing pat­terns and sexual sys­tems in flower­ing plants has fas­cin­ated evol­u­tion­ary bio­lo­gists for more than a cen­tury. Enduring ques­tions about this topic include why sexual poly­morph­isms have evolved inde­pend­ently in over 100 plant fam­il­ies, and why pro­por­tions of self– and cross-fertilization often vary dra­mat­ic­ally within and among pop­u­la­tions. Important new insights con­cern­ing the evol­u­tion­ary dynam­ics of plant mat­ing sys­tems have built upon a strong found­a­tion of the­or­et­ical mod­els and innov­at­ive field and labor­at­ory exper­i­ments. However, as the pace of advance­ment in this field has accel­er­ated, it has become increas­ingly dif­fi­cult for research­ers to fol­low devel­op­ments out­side their primary area of research expertise.

In this issue we high­light three import­ant themes that span and integ­rate dif­fer­ent sub­dis­cip­lines: the changes in mor­pho­logy, phen­o­logy, and physiology that accom­pany the trans­ition to self­ing; the evol­u­tion­ary con­sequences of pol­len pool diversity in flower­ing plants; and the evol­u­tion­ary dynam­ics of sexual poly­morph­isms. We also high­light recent devel­op­ments in molecu­lar tech­niques that will facil­it­ate more effi­cient and cost-effective study of mat­ing pat­terns in large nat­ural pop­u­la­tions, research on the dynam­ics of pol­len trans­port, and invest­ig­a­tions on the genetic basis of sexual polymorphisms.


Mathilde Dufay and Emmanuelle Billard
How much bet­ter are females? The occur­rence of female advant­age, its prox­imal causes and its vari­ation within and among gyn­odi­oecious species.

Theoretically, females should be able to coex­ist with herm­aph­rod­ites only if they bene­fit from a repro­duct­ive advant­age. By review­ing and ana­lys­ing data pub­lished on 48 spe­cies, Dufay and Billard (pp. 505–519) show that this expect­a­tion is usu­ally true; how­ever, the mag­nitude of the advant­age shows con­sid­er­able vari­ation among, and some­times within, spe­cies, and its prox­imal causes vary from one spe­cies to another. They sug­gest that reduced self­ing may not be the major cause of the occur­rence of female advant­age, and thus of the main­ten­ance of gynodioecy.

Glenda Vaughton and Mike Ramsey
Gender plas­ti­city and sexual sys­tem sta­bil­ity in Wurmbea

Gender plas­ti­city in herm­aph­rod­ites is pro­posed to influ­ence the evol­u­tion of sep­ar­ate sexes. Vaughton and Ramsey (pp. 521–530) char­ac­ter­ize gender plas­ti­city in herm­aph­rod­ites and uni­sexu­als under dif­fer­ent resource con­di­tions in two Wurmbea spe­cies with sexual sys­tems ran­ging from cosexu­al­ity to dioecy. They find that herm­aph­rod­ites pro­duce fewer per­fect flowers, but not stam­in­ate flowers, when resources are reduced; uni­sexu­als are unaf­fected. This study high­lights the import­ance of inter­ac­tions between the envir­on­ment and herm­aph­rod­ite gender expres­sion for the sta­bil­ity of sexual systems.

Rachel B. Spigler and Tia-Lynn Ashman
Gynodioecy to dioecy: are we there yet?

The trans­ition from com­bined sexes (herm­aph­rod­it­ism) to sep­ar­ate sexes (dioecy) is a fun­da­mental one in flower­ing plants. Evidence and sub­sequent under­stand­ing of how females invade and estab­lish in herm­aph­rod­itic pop­u­la­tions at the begin­ning of the ‘gynodioecy–dioecy path­way’ is rich com­pared to that for later stages, wherein males invade and sup­plant herm­aph­rod­ites. Spigler and Ashman (pp. 531–543) review exist­ing evid­ence for the lat­ter part of the path­way and dis­cuss how major eco­lo­gical factors can influ­ence these dynamics.

Junmin Li, Matthew H. Koski, and Tia-Lynn Ashman
Functional char­ac­ter­iz­a­tion of gyn­odi­oecy in Fragaria vesca ssp. bracteata (Rosaceae)

Gynodioecy is a phylo­gen­et­ic­ally wide­spread sexual sys­tem where females coex­ist with herm­aph­rod­ites. Because dioecy can arise from gyn­odi­oecy, char­ac­ter­iz­a­tion of gyn­odi­oecy in close rel­at­ives of dioecious and sub­di­oecious spe­cies can provide insights into this trans­ition. Li et al. (pp. 545–552) report func­tional evid­ence of gyn­odi­oecy in Fragaria vesca ssp. bracteata, the only dip­loid Fragaria spe­cies that is not herm­aph­rod­itic. While the sex morphs alloc­ate sim­il­arly to repro­duc­tion, herm­aph­rod­ites are highly self­ing in the field and their pro­geny are less likely to ger­min­ate, sug­gest­ing inbreed­ing depres­sion as a poten­tial driver of female main­ten­ance. Compared to sub­di­oecious and dioecious con­gen­ers, sexual dimorph­ism in this gyn­odi­oecious spe­cies is less pronounced.

Jeremiah W. Busch and Lynda F. Delph
The rel­at­ive import­ance of repro­duct­ive assur­ance and auto­matic selec­tion as hypo­theses for the evol­u­tion of self-fertilization

Many pos­sible mech­an­isms drive the evol­u­tion­ary trend from out­cross­ing to self­ing, but most research has focused upon the trans­mis­sion advant­age of self­ing and its abil­ity to provide repro­duct­ive assur­ance when cross-pollination is uncer­tain. Busch and Delph (pp. 553–562) dis­cuss the shared con­cep­tual frame­work of these ideas and their empir­ical sup­port that is emer­ging from tests of their pre­dic­tions over the last 25 years. They con­clude that although repro­duct­ive assur­ance appears likely as a lead­ing factor facil­it­at­ing the evol­u­tion of self­ing, stud­ies must account for both seed and pol­len dis­count­ing to adequately test this hypothesis.

Jeffrey D. Karron and Randall J. Mitchell
Effects of floral dis­play size on male and female repro­duct­ive suc­cess in Mimulus ringens

The num­ber of flowers bloom­ing sim­ul­tan­eously on a Mimulus ringens plant often var­ies markedly within pop­u­la­tions. By com­bin­ing floral dis­play manip­u­la­tions with unam­bigu­ous patern­ity assign­ment, Karron and Mitchell (pp. 563–570) demon­strate that an increase in dis­play size leads to a dra­matic reduc­tion in out­cross sir­ing suc­cess per flower, but only a mod­est increase in self­ing. Their res­ults sug­gest that pol­len dis­count­ing may play a crit­ical role in the evol­u­tion of floral dis­play strategies.

Susan Kalisz, April Randle, David Chaiffetz, Melisa Faigeles, Aileen Butera, and Craig Beight
Dichogamy cor­rel­ates with out­cross­ing rate and defines the self­ing syn­drome in the mixed-mating genus Collinsia

Collinsia is a genus of self-compatible mixed-mating spe­cies that dif­fer markedly in floral mor­pho­lo­gical and devel­op­mental traits asso­ci­ated with mat­ing sys­tem vari­ation. Kalisz et al. (pp. 571–582) find that the pres­ence or absence of dicho­gamy is dia­gnostic of self­ing and out­cross­ing syn­dromes. However, spe­cies in both syn­drome groups express equal and high rates of autonom­ous self­ing in the absence of pol­lin­at­ors and highly vari­able self­ing rates in nature. This points to the crit­ical influ­ence of the pol­lin­a­tion envir­on­ment and the lab­il­ity of dicho­gamy for mat­ing sys­tem evol­u­tion of this clade.

Christopher T. Ivey and David E. Carr
Tests for the joint evol­u­tion of mat­ing sys­tem and drought escape in Mimulus

Self-fertilization may be dir­ectly selec­ted or may evolve indir­ectly through selec­tion on other traits with which it is cor­rel­ated. Ivey and Carr (pp. 583–598) test the hypo­thesis that self­ing in the genus Mimulus evolved jointly with traits that allow plants to avoid expos­ure to sea­sonal drought. Under field and con­trolled drought con­di­tions they meas­ure phen­o­typic and genetic responses of drought escape and mat­ing sys­tem traits. Although some meas­ured traits are incon­sist­ent with the hypo­thesis, sev­eral plastic responses to soil mois­ture treat­ments sup­port the idea that taxo­nomic diver­gence could have been facil­it­ated by plas­ti­city in flower­ing time and self­ing, and fur­ther study is warranted.

Sara R. Dart, Karen E. Samis, Emily Austen, and Christopher G. Eckert
Broad geo­graphic cov­ari­ation between floral traits and the mat­ing sys­tem in Camissoniopsis cheir­anthi­fo­lia (Onagraceae): mul­tiple stable mixed mat­ing sys­tems across the spe­cies’ range?

Plants vary widely in the extent to which seeds are pro­duced via self-fertilization vs. out­cross­ing, but whether there are dis­tinct stable end­points of mat­ing sys­tem evol­u­tion is unre­solved. Dart et al. (pp. 599–611) ana­lyse geo­graphic vari­ation in floral traits together with genetic mat­ing sys­tem estim­ates for the coastal dune endemic Camissoniopsis cheir­anthi­fo­lia (Onagraceae) and show that the trans­ition to com­plete self­ing has not occurred even though the spe­cies appears to pos­sess the required genetic capa­city. Instead they hypo­thes­ize that out­cross­ing pop­u­la­tions in this spe­cies have evolved to dif­fer­ent stable states of mixed mating.

Donald A. Levin
Mating sys­tem shifts on the trail­ing edge

The trail­ing edges of spe­cies’ ranges are becom­ing a sub­ject of increas­ing interest as the envir­on­ment changes due to global warm­ing. In this review, Levin (pp. 613–620) notes that small pop­u­la­tions on the trail­ing edge will prob­ably exper­i­ence low levels of cross-pollination, and hence indi­vidu­als that are self-compatible and are cap­able of self-pollination will be at an advant­age. By vir­tue of the repro­duct­ive assur­ance it con­fers, sys­tem­atic degrad­a­tion of the envir­on­ment will thus favour the elev­a­tion of self-fertility, which may arise in the short term through devel­op­mental responses to stress or in the longer term by changes in the self-incompatibility locus or genes that affect the beha­viour of this locus. However, self­ing will also lead to sub­stan­tial reduc­tions in genetic diversity, which may render adapt­a­tion unlikely.

C. J. Murren and M. R. Dudash
Variation in inbreed­ing depres­sion and plas­ti­city across nat­ive and non-native field environments

Inbreeding depres­sion and plas­ti­city have been hypo­thes­ized to be crit­ical to ini­tial estab­lish­ment suc­cess of pop­u­la­tions in novel envir­on­ments. Comparing the per­form­ance of out­crossed and inbred lines of Mimulus gut­tatus across nat­ive and novel field sites, Murren and Dudash (pp. 621–632) find that inbreed­ing depres­sion and phen­o­typic plas­ti­city vary among field sites. Outcrossed off­spring gen­er­ally out­per­form selfed off­spring, yet in the native-novel site self-progeny per­form bet­ter or equally well as out­cross pro­geny. Evidence is detec­ted for greater plas­ti­city to novel sites and an inter­ac­tion between inbreed­ing and plas­ti­city, sug­gest­ing the import­ance of both responses out­side a spe­cies’ cur­rently inhab­ited range.

P.-O. Cheptou
Clarifying Baker’s Law

Baker’s Law states that col­on­iz­a­tion by self-compatible organ­isms is more likely to be suc­cess­ful than col­on­iz­a­tion by self-incompatible organ­isms because of the abil­ity of self-compatible organ­isms to pro­duce off­spring without pol­lin­a­tion agents. Cheptou (pp. 633–641) reviews data and con­cepts relat­ing to Baker’s Law and con­cludes that it is not totally com­pat­ible with mat­ing sys­tem mod­els based on a pop­u­la­tion genetic per­spect­ive, which assess ‘fit­ness’ in terms of genes trans­mit­ted rather than from the more demo­graphic view taken by Baker. There is a need to char­ac­ter­ize colonization/extinction dynam­ics, i.e. meta­pop­u­la­tion scen­arios, in order to inter­pret selec­tion processes.

Andrew G. Young, Linda M. Broadhurst, and Peter H. Thrall
Non-additive effects of pol­len lim­it­a­tion and self-incompatibility reduce plant repro­duct­ive suc­cess and pop­u­la­tion viability

Pollen lim­it­a­tion and loss of self-incompatibility gen­o­types can both act inde­pend­ently to reduce seed set in frag­men­ted land­scapes. Young et al. (pp. 643–653) use a sim­u­la­tion model to exam­ine effects of pol­len lim­it­a­tion and loss of self-incompatibility alleles on the repro­duct­ive suc­cess and pop­u­la­tion viab­il­ity of a short-lived per­en­nial herb. They find that pop­u­la­tion decline may occur more rap­idly than expec­ted when pol­lin­a­tion prob­ab­il­it­ies drop below 25 % and S alleles are fewer than 20 due to non-additive inter­ac­tions. These are likely to be com­mon con­di­tions exper­i­enced by plants in small pop­u­la­tions in frag­men­ted landscapes.

V. Ferrero, J. Arroyo, S. Castro, and L. Navarro
Unusual het­ero­styly: style dimorph­ism and self-incompatibility are not tightly asso­ci­ated in Lithodora and Glandora (Boraginaceae)

Heterostyly is char­ac­ter­ized by the recip­rocal pos­i­tion of sta­mens and stig­mas in dif­fer­ent flower morphs, and is usu­ally asso­ci­ated with an incom­pat­ib­il­ity sys­tem that pre­vents self­ing and intra-morph cross-fertilization. Ferrero et al. (pp. 655–665) exam­ine incom­pat­ib­il­ity sys­tems in Lithodora and Glandora (Boraginaceae), which have dif­fer­ent stylar poly­morph­isms, and recon­struct a phylo­geny of these gen­era and related spe­cies. They con­clude that stylar poly­morph­ism and the incom­pat­ib­il­ity sys­tem appear to have evolved inde­pend­ently in this group of plants, which con­trasts with the ortho­dox view that there is strong link­age between these repro­duct­ive traits.

Caroli de Waal, Bruce Anderson, and Spencer C. H. Barrett
The nat­ural his­tory of pol­lin­a­tion and mat­ing in bird-pollinated Babiana (Iridaceae)

Bird pol­lin­a­tion has ori­gin­ated in many angio­sperm lin­eages but little is known about the mat­ing bio­logy of sunbird-pollinated plants. De Waal et al. (pp. 667–679) invest­ig­ate the floral eco­logy of four spe­cies of Babiana (Iridaceae) endemic to the Cape region of South Africa. This group is of spe­cial interest because sev­eral pos­sess the most spe­cial­ized bird perch known in the plant king­dom. Using genetic mark­ers they demon­strate self-fertilization in all pop­u­la­tions, indic­at­ing that pol­lin­ator spe­cial­iz­a­tion is not always asso­ci­ated with cross-fertilization, as is often assumed.

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