Spermatozoon ultrastructure and spermiogenesis are significant characters for phylogenetic inference. Sperm ultrastructure is reviewed from the literature in 56 species of Eucestoda. Data are available for 11 of the 12 orders of Eucestoda (Lecanicephalidea excepted), but in some orders data are scarce and often limited to a single species. Spermiogenesis and sperm ultrastructure in the Eucestoda is compared to that of other parasitic Platyhelminthes, with emphasis on structures of phylogenetic interest. Not only the descriptions of sperm structure, but those of the process of spermiogenesis, are necessary to define characters. Synapomorphies based on sperm ultrastructure for the Eucestoda include the absence of a mitochondrion in mature sperm and the presence of a crested body. A proposed synapomorphy for the Cyclophyllidea + Tetrabothriidea is the twisting of the peripheral microtubules; the absence of intercentriolar body and the absence of striated roots in the spermatid may constitute additional synapomorphies for this assemblage. Absence of flagellar rotation during spermiogenesis is synapomorphic for the Cyclophyllidea, and absence of proximodistal fusion could be synapomorphic for a part of the Cyclophyllidea. Several other characters could be useful for understanding phylogeny within the Eucestoda. The polarity of these characters could in several cases be determined, but diagnoses for taxa or relationships based on synapomorphies cannot be specified unequivocally due to putative convergence. Such characters and their putative polarity include: (1) the number of axonemes in mature spermatozoon (plesiomorphic=2; apomorphic=1); (2) size and number of crested bodies (p=1; a=several); and (3) angle of twisted microtubules; shape of nucleus (p=compact cord; a=crescent and annulus). Additional apomorphic attributes include (1) presence of a periaxonemal sheath (a putative synapomorphy for the Cyclophyllidea + Tetrabothriidea if reversals are postulated in certain cyclophyllideans); (2) presence of proteinaceous transverse walls; (3) presence of dense granules; and (4) shape of apical cones and posterior structures. Studies of sperm structure in the poorly known orders and additional comparative studies in the Cyclophyllidea are expected to provide new information for elucidation of phylogenetic relationships.

The phylogeny of the Eucestoda was evaluated based on a suite of 49 binary and multistate characters derived from comparative morphological and ontogenetic studies; attributes of adult and larval tapeworms were considered. A single most parsimonious tree (MPT) (consistency index = 0.872; retention index = 0.838; and homoplasy index = 0.527) was fully resolved and is specified by the following: (Gyrocotylidea, (Amphilinidea, ((Spathebothriidea, (Pseudophyllidea, ((Diphyllidea, (Trypanorhyncha, (Tetraphyllidea, (Lecanicephalidea, ((Nippotaeniidea, (Tetrabothriidea, Cyclophyllidea)), Proteocephalidea))))), Haplobothriidea))), Caryophyllidea))). Monophyly for the Eucestoda was firmly corroborated. Trees derived from the primary and bootstrap analyses were congruent, but low values, particularly for relationships among the tetrafossate tapeworms, indicated additional examination is warranted. The MPT was found to be the most efficient hypothesis for describing character evolution and in specifying relationships among the orders when compared to those concepts that had been developed for the tapeworms over the past century. Areas of congruence were shared among the current hypothesis and one or more of the prior hypotheses. Major conclusions include: (1) Caryophyllidea are basal and monozooy is ancestral; (2) difossate forms are primitive, and the Pseudophyllidea are the sister group of the strongly polyzoic tapeworms; (3) Nippotaeniidea are highly derived; (4) the higher tapeworms (Tetraphyllidea, Lecanicephalidea, Proteocephalidea, Nippotaeniidea, Tetrabothriidea, and Cyclophyllidea) are closely related or potentially coordinate groups; (5) Tetrabothriidea and the Cyclophyllidea are sister groups; and (6) Tetraphyllidea is paraphyletic, with the Onchobothriidae basal to the Phyllobothriidae. Character support for placement of the Tetrabothriidea continues to be contradictory, and this order may represent a key to understanding the phylogeny of the higher cestodes. The current study constitutes a complete historical review and poses a new and robust hypothesis for the phylogeny of the Eucestoda.