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Female duck anatomy evolves to block “rape

May 1, 2007
Courtesy Yale University
and World Science staff

Bi­ol­o­gists have found ana­tom­i­cal de­tails about the fe­male re­pro­duc­tive tract in wa­ter­fowl that they say in­di­cate male and fe­male an­atomy have co-e­volved in a “sex­ual arms race.”

Bird cop­u­la­tion most­ly con­sists of a sim­ple, and rath­er chaste, “cloa­cal kiss” in which two open­ings come to­ge­ther. But a few an­cient bird lin­eages, in­clud­ing wa­ter­fowl, re­tain the grooved phal­lus of their rep­til­i­an an­ces­tors. Wa­ter­fowl are al­so dis­tinct in hav­ing great di­ver­si­ty among spe­cies in the length and or­na­men­ta­tion of the phal­lus.

Sci­en­tists pre­vi­ously at­trib­ut­ed this di­ver­si­ty to sperm com­pe­ti­tion. They spec­u­lat­ed that sperm from ma­les with a long­er phal­lus had a com­pet­i­tive edge over sperm from those less well-en­dowed. The new re­port in the on­line re­search jour­nal PLoS One finds more to the sto­ry. 

“As part of a re­search pro­gram on the ev­o­lu­tion of the avi­an phal­lus, I was cu­ri­ous to know if there were con­se­quenc­es to fe­male ducks of the tre­men­dous ana­tom­i­cal var­i­a­tion found in the male phal­lus,” said lead au­thor Pa­tri­cia Bren­nan of Yale Uni­ver­si­ty in New Hav­en, Conn. and the Uni­ver­si­ty of Shef­field, U.K. 

Her study is a com­ple­men­tary ex­plo­ra­tion of the an­atomy of the fe­male re­pro­duc­tive tract, called the ov­i­duct or va­gi­na, which is usu­al­ly very sim­ple and si­m­i­lar among birds. Bren­nan found two un­ex­pect­ed­ly com­plex and new struc­tures that she said seem de­signed for one pur­pose — to se­lec­tive­ly ex­clude the phal­lus.

In most birds, the ov­i­duct is a sim­ple tube, but in some wa­ter­fowl, the tube has unique sacs and spi­rals. The sacs are out­po­cket­ings in the sides of the tube that are just in­side the ov­i­duct open­ing. “They ap­pear to func­tion as ‘dead-ends,’ or false pas­sages,” said Bren­nan. “If the phal­lus were to en­ter one of these sacs, it would not prog­ress fur­ther in­to the ov­i­duct where it would de­pos­it sperm more ef­fec­tive­ly.”

The sec­ond nov­el­ty is a se­ries of tight, clock-wise spi­rals in the tub­u­lar ov­i­duct. “In­ter­est­ingly, the male phal­lus is al­so a spir­al, but it twists in the op­po­site, counter-clockwise, di­rec­tion,” said Yale or­ni­thol­o­gist and co-au­thor Rich­ard Prum. “So the twists in the ov­i­duct ap­pear de­signed to ex­clude the op­pos­ing twists of the male phal­lus.” 

The num­ber of sacs and spi­rals in the re­pro­duc­tive tract of var­i­ous fe­male wa­ter­fowl cor­re­lates strongly with the length of the male phal­lus, the sci­ent­ists wrote. 

Com­par­ing the phal­lus size and ov­i­duct shape in 14 dif­fer­ent spe­cies of ducks and geese, the au­thors con­c­luded that the gen­i­ta­lia of ma­les and fe­ma­les have dy­nam­i­cal­ly co-e­volved: in var­i­ous se­parate duck lin­eages, fe­males de­vel­oped more elab­o­rate ov­i­ducts as males evolved long­er phal­luses. In oth­er lin­eages fe­males lost ov­i­duct com­plexity as the phal­lus evolved to­ward smal­ler size. 

Bren­nan hy­poth­e­sizes that the fe­male wa­ter­fowl have evolved these ana­tom­i­cal fea­tures to block male at­tempts at re­pro­duc­tive con­trol. “De­spite the fact that most wa­ter­fowl form mo­nog­a­mous pairs, forced cop­u­la­tions by oth­er ma­les — the avi­an equiv­a­lent of rape — are com­mon in many wa­ter­fowl,” said Prum. “The length of the phal­lus of a spe­cies is strongly cor­re­lat­ed with the fre­quen­cy of forced cop­u­la­tions.” 

“In re­sponse to male at­tempts to force their pa­ter­ni­ty on fe­ma­les, fe­male wa­ter­fowl may be able to as­sert their own be­hav­ior­al and ana­tom­i­cal means of con­trolling who fa­thers their off­spring,” Bren­nan said. 

The au­thors pro­pose that ornate phal­luses and fe­male ov­i­ducts have co-e­volved in re­sponse to one an­oth­er. More elab­o­rate phal­luses have se­lected for im­proved means of ex­clud­ing them, and vi­ce versa. 

What hap­pens when a fe­male duck wants to mate with its cho­sen part­ner? The au­thors spec­u­late that these phys­i­cal bar­ri­ers are eas­i­ly overcome when fe­ma­les co­op­er­ate, and that they only func­tion to ex­clude un­want­ed ad­vanc­es. Bren­nan is pur­su­ing the find­ings with fur­ther ex­plo­ra­tion of the de­vel­op­ment and ev­o­lu­tion of bird gen­i­ta­lia. “I am sure there are more sur­prises out there,” she said.


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Biologists have found ana tomical details about the female reproductive tract in waterfowl that they say indicate male and female anatomy have co-evolved in a “sexual arms race.” Birds copulation mostly consists of a simple, and rather chaste, “cloacal kiss” in which two openings come into contact. But a few ancient bird lineages, including waterfowl, retain the grooved phallus found in their reptilian ancestors. Waterfowl are also distinct in having great diversity among different species in the length and ornamentation of the phallus. Scientists previously attributed this diversity to sperm competition. They speculated that sperm from males with a longer phallus had a competitive edge over sperm from those less well-endowed. The new report in the online journal PLoS ONE finds more to the story. “As part of a research program on the evolution of the avian phallus, I was curious to know if there were consequences to female ducks of the tremendous ana tomical variation found in the male phallus,” said lead author Patricia Brennan of Yale University in New Haven, Conn. and the University of Sheffield, U.K. Her study is a complementary exploration of the anatomy of the female reproductive tract, called the oviduct or vagina, which is usually very simple and similar among birds. Brennan found two unexpectedly complex and new structures that all seem designed for one purpose — to selectively exclude the male phallus. In most birds, the oviduct is a simple tube, but in some waterfowl, the tube has unique sacs and spirals. The sacs are out-pocketings in the sides of the tube that are just inside the opening of the oviduct. “They appear to function as ‘dead-ends,’ or false passages,” said Brennan. “If the phallus were to enter one of these sacs, it would not progress further into the oviduct where it would deposit sperm more effectively.” The second structural novelty of the female is a series of tight, clock-wise spirals in the tubular oviduct. “Interestingly, the male phallus is also a spiral, but it twists in the opposite, counter-clockwise, direction,” said Yale ornithologist and co-author Richard Prum. “So, the twists in the oviduct appear designed to exclude the opposing twists of the male phallus. It’s an exquisite anti-lock-and-key system.” The number of sacs and spirals in the reproductive tract of various female waterfowl correlates strongly with the length of the male phallus. Comparing the phallus size and oviduct shape in 14 different species of ducks and geese, the authors show that the genitalia of males and females have dynamically co-evolved with one another. According to the study, in various independent lineages of ducks females developed more elaborate oviducts as males evolved longer phalluses. In other lineages females lost oviduct complexity as the phallus evolved toward smaller size. Why all this dynamic evolution? Brennan hypothesizes that the female waterfowl have evolved these unique ana tomical features as physical counter-measures to evade male attempts to assert control over reproduction. “Despite the fact that most waterfowl form monogamous pairs, forced copulations by other males — the avian equivalent of rape — are common in many waterfowl,” said Prum. “The length of the phallus of a species is strongly correlated with the frequency of forced copulations.” “In response to male attempts to force their paternity on females, female waterfowl may be able to assert their own behavioral and ana tomical means of controlling who fathers their offspring,” Brennan said. Consequently, the authors propose that elaborate phalluses and female oviducts have co-evolved in a dynamic response to one another. Phalluses that are more elaborate have selected for improved means of excluding them, and vice versa. What happens when a female duck wants to mate with its chosen partner? The authors speculate that these physical barriers are easily overcome when females cooperate during copulation, and that they only function to exclude unwanted advances. Brennan is pursuing these results with further exploration of the development and evolution of genitalia in birds. “I am sure there are more surprises out there,” she said.