The Evolutionary Implications of Hemipenial Morphology of Rattlesnake Crotalus durissus terrificus (Laurent, 1768) (Serpentes: Viperidae: Crotalinae)
1768) (Serpentes: Viperidae: Crotalinae). PLoS ONE 8(6): e66903. doi:10.1371/journal.pone.0066903
The Evolutionary Implications of Hemipenial Morphology of Rattlesnake Crotalus durissus terrificus (Laurent, 1768) (Serpentes: Viperidae: Crotalinae)
Marcovan Porto 0
Marco Antonio de Oliveira 0
Lorenzo Pissinatti 0
Renata Lopes Rodrigues 0
Julio Alejandro Rojas-Moscoso 0
Jose Carlos Cogo 0
Konradin Metze 0
Edson Antunes 0
Ce sar Nahoum 0
Fabola Z. Mo nica 0
Gilberto De Nucci 0
John Wallace, McMaster University, Canada
0 1 Department of Pharmacology, Faculty of Medical Sciences, State University of Campinas , Campinas, Sa o Paulo , Brazil , 2 Institute of Research and Development, University of Vale do Para ba (UNIVAP) Sa o Jose dos Campos, Sa o Paulo, Brazil, 3 Department of Pathology, Faculty of Medical Sciences, State University of Campinas , Campinas, Sa o Paulo , Brazil , 4 Department of Pharmacology, Institute of Biomedical Sciences, University of Sa o Paulo (USP), Sa o Paulo , Sa o Paulo , Brazil
Most amniotes vertebrates have an intromittent organ to deliver semen. The reptile Sphenodon and most birds lost the ancestral penis and developed a cloaca-cloaca mating. Known as hemipenises, the copulatory organ of Squamata shows unique features between the amniotes intromittent organ. They are the only paired intromittent organs across amniotes and are fully inverted and encapsulated in the tail when not in use. The histology and ultrastructure of the hemipenes of Crotalus durissus rattlesnake is described as the evolutionary implications of the main features discussed. The organization of hemipenis of Crotalus durissus terrificus in two concentric corpora cavernosa is similar to other Squamata but differ markedly from the organization of the penis found in crocodilians, testudinata, birds and mammals. Based on the available data, the penis of the ancestral amniotes was made of connective tissue and the incorporation of smooth muscle in the framework of the sinusoids occurred independently in mammals and Crotalus durissus. The propulsor action of the muscle retractor penis basalis was confirmed and therefore the named should be changed to musculus hemipenis propulsor.The retractor penis magnus found in Squamata has no homology to the retractor penis of mammals, although both are responsible for the retraction of the copulatory organ.
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Funding: Financial support FAPESP (Grant #2011/11828-4) Fundacao de Amparo a Pesquisa do Estado de Sao Paulo (http://www.fapesp.br). JARM, LP, MP and
MAdO have fellowships from CNPq. FZM has a fellowship from FAPESP. The funders had no role in study design, data collection and analysis, decision to publish,
or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
The intromittent organs are functional structures of male
organisms with the main function of gamete delivery. They are an
adaptation usually observed in organisms that require internal
fertilization, and have arisen multiple times in a number of
vertebrate and invertebrate lineages [1]. Although the internal
fertilization is a synapomorphy to Amniotes vertebrates, most birds
and the reptile Sphenodon lack intromittent organs and transfer
sperm by cloacal apposition [2].
The intromittent organ of Amniotes vertebrate must be an
efficient mechanism for transferring spermatozoon to cloaca or
vagina of the female [3]. It must be to stiff enough to penetrate the
vulva without bending during copulation [1,3] The corpora cavernosa
seen arises in amniotes to supply this function, first as a simply
hydraulic machine that becomes enlarged by blood. As amniotes
form a monophyletic group, we can expect a similar arrange in the
penis general morphology. The penile morphology of mammals,
which is an integrated part of the complex physiology of male
sexual behavioral, varies greatly among the distinct species [47].
The widely prevalent description of the mammal corpora cavernosa is
that they are composed of prominent vascular spaces (also known
as sinusoidal, lacunar spaces or cave), separated by incomplete
fibromuscular trabeculae, rich in smooth muscle [8,9]. Each
hollow shows incomplete fibromuscular trabeculae, rich in smooth
muscle. The relaxation and contraction of the smooth muscle
controls the erection and detumescence, respectively, of the
mammal penis. In birds [2,10], crocodiles [2], turtles [3,11],
Lacerta agilis [12] and some snakes [1315], the corpora cavernosa is
formed by fibrous elastic connective tissue. Bundles of muscle are
generally absent in penis of this group, but was noted in rattlesnake
Crotalus durissus cascavella [16], in Crotalus durissus terrificus [17], in
amphisbaenid [18] and Uroastix hardwickii lizard [19]. These
differences seem to support that penis has evolved independently
at least three to four times in amniotes, specifically in mammals,
turtles, Squamata, crocodiles, and the Paleognathes and
Galloanseridae birds [2,10].
The m (...truncated)