The male sexual apparatus in the order Scorpiones (Arachnida): a comparative study of functional morphology as a tool to define hypotheses of homology

Abstract

BackgroundInsemination in scorpions is carried out by means of a partly sclerotized structure, the spermatophore, which is composed of two separate halves, the hemispermatophores. In most genera these reproductive structures can be used to differentiate species. However, many taxa such as the genus Euscorpius and the family Diplocentridae lack the morphological diversity observed in the copulatory organs of many other arthropods, rendering them useless for species level taxonomy. Such structural stasis, however, suggests that hemispermatophores have evolved relatively slowly and may thus provide a stronger phylogenetic signal for recognizing supra-generic ranks than previously thought. Based on the postulate that the phenotypic stability observed in some groups is the consequence of functional constraint, the most comprehensive comparative study of the male sexual apparatus to date was conducted for a complete reassessment of the morphology, phylogenetic value and hypotheses of homology of these structures.ResultsHemispermatophores, pre- and post-insemination spermatophores, as well as the inherent mechanisms of insemination, were studied across the whole order, allowing the recognition and description of a series of five basic bauplans for the capsular region. For the most part, these patterns appear to be consistent within each major taxonomic group, but several cases of incongruence between spermatophore morphology and taxonomy raises questions about the monophyly of some clades. The Bothriuridae are traditionally regarded as a basal scorpionoid family. However, except for the genus Lisposoma, bothriurid hemispermatophores and spermatophores are morphologically more similar to those of the Chactoidea than to those of scorpionoids. On the other hand, the male copulatory structures of the hormurid clade (Hormiops (Hormurus + Liocheles)) are more akin to those of Diplocentridae and Heteroscorpionidae than to those of other hormurids.ConclusionsSpermatophore capsular patterns appears to be congruent with a recent phylogeny of the order Scorpiones based on phylogenomic data that placed Bothriuridae outside of Scorpionoidea and Liocheles outside of Hormuridae, in contradicton with earlier phylogenetic reconstructions based on morphology. This raises questions about the potential use of functionally constrained traits to assess the reliability of contradicting phylogenetic hypotheses and emphasizes the need for a thorough reassessment of the scorpion phylogenetic relationships.Electronic supplementary materialThe online version of this article (10.1186/s12983-017-0231-z) contains supplementary material, which is available to authorized users.

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“…HEMISPERMATOPHORES. The chaerilid hemispermatophores documented here are similar to those previously reported for the family (Bastawade, 1994;Kovařík et al, 2015;Lourenço & Duhem, 2010;Monod et al, 2017;Stockwell, 1989). All conform to the basic plan of a laterally compressed fusiform structure with relatively large capsule region, relatively short, broad trunk, and a short, posteriorly directed distal lamina.…”

Scorpions of the Horn of Africa (Arachnida: Scorpiones). Part XV. Review of the genus Gint Kovařík et al., 2013, with description of three new species from Somaliland (Scorpiones, Buthidae)

“…Kovařík et al, 2016c). Along the transverse axis, following Stockwell (1989) and Monod et al (2017), opposing hemispermatophore mar-gins bearing the sperm hemiduct and flagellum are referred to as 'anterior' and 'posterior' respectively, based on orientation of formed spermatophores when attached to the substrate, referred to the somatic axes of males positioned during mating with females. Surfaces that become interior or exterior in formed spermatophores are 'concave' and 'convex' respectively, terms that are self-explanatory.…”

“…The three lobes of the sperm hemiduct are labelled as 'anterior', 'median' and 'posterior' lobes, according to the above transverse axis convention (='external', 'median' and 'interior' lobes respectively of Vachon, 1940Vachon, , 1952. We continue using the generic term 'basal lobe' rather than 'basal hook' (Monod et al, 2017), because this process may not be shaped like a hook.…”

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“…She envisaged sperm being ejected as the male rocked the female back and forth while the enlarged basal pectine structures held the basal lobes, compressing the trunk. However, the basal lobes are too distal to permit such a function (Monod et al, 2017). Alternatively, the enlarged teeth or middle lamellae may serve either to directly embrace, or to impose constraints on lateral flexure of the spermatophore trunk, preventing it from bending too far sideways during rocking.…”