Reproductive histology of Tomeurus gracilis Eigenmann, 1909 (Teleostei: Atherinomorpha: Poeciliidae) with comments on evolution of viviparity in atherinomorph fishes

Abstract

Tomeurus gracilis is a species long considered pivotal in understanding the evolution of livebearing in atherinomorph fishes. Tomeurus gracilis is a zygoparous or embryoparous poeciliid: internal fertilization is followed by females laying fertilized eggs singly or retaining fertilized eggs until or near hatching. Tomeurus was hypothesized as the sister group of the viviparous poeciliids until it was proposed as a close relative of a derived viviparous poeciliid, Cnesterodon, hence nested among viviparous taxa rather than near the root of the tree. Here, we describe and compare reproductive morphological characters of the little-known Tomeurus with those of representative atherinomorphs. In Tomeurus and Cnesterodon, sperm are packaged in naked sperm bundles, or spermatozeugmata, in a configuration considered here diagnostic of viviparous poeciliids. Testes are single and free sperm are stored in the ovary in both taxa in contrast to oviparous atherinomorphs in which testes are paired and sperm are not packaged and not stored in the ovary. Efferent ducts in Cnesterodon testes and other viviparous poeciliids have a PAS-positive secretion demonstrating presence of a glycoprotein that inactivates sperm or prevents final sperm maturation. No PAS-positive staining secretion was observed in Tomeurus or oviparous atherinomorphs. Tomeurus shares apomorphic reproductive characters, such as sperm bundle and testis morphology and a gonopodium, with viviparous poeciliids and plesiomorphic characters, such as a thick zona pellucida with filaments, with oviparous taxa. We do not postulate loss or reversal of viviparity in Tomeurus, and we corroborate its phylogenetic position as sister to the viviparous poeciliids.

Structure of the testis and spermatogenesis of the viviparous teleost Poecilia mexicana (Poeciliidae) from an active sulfur spring cave in Southern Mexico

“…The histological analysis showed that the testicular structure and spermatogenesis of the restricted spermatogonial testis type of P. mexicana are similar to these described in other poeciliids such as G. affinis holbrooki (Fraile et al, 1992), Poecilia sphenops, P. latipinna (Grier, 1975;Grier et al, 1980;, P. reticulata (Billard, 1969;Pandey, 1969;Vaupel, 1929), and Tomeurus gracilis (Parenti, LoNostro, & Grier, 2010). This testis type has been described not only in poeciliids, but in all members of the orders Atheriniformes, Cyprinodontiformes, and Beloniformes (Parenti & Grier, 2004).…”

Morphological specializations for fetal maintenance in viviparous vertebrates: An introduction and historical retrospective

“…Among papers that have appeared in the Journal of Morphology are several "firsts" that warrant mention. These include the following: one of the Grove and Wourms, 1991 Follicular placenta Heterandria formosa (Poeciliidae) Grove and Wourms, 1994 Follicular placenta Heterandria formosa (Poeciliidae) Hollenberg and Wourms, 1994 Trophotaeniae, matrotrophy Goodeidae Jollie and Jollie, 1964a Pregnant ovarian follicle Lebistes reticulatus (Poeciliidae) Jollie and Jollie, 1964b Follicular placenta Lebistes reticulatus (Poeciliidae) Kokkala and Wourms, 1994 Trophotaenial placenta Goodeidae Knight et al, 1985 Follicular placenta, development Anableps (Anablepidae) Kwan et al, 2015 Follicular placenta Poeciliopsis (Poeciliidae) Lombardi and Wourms, 1985a Trophotaenial placenta Ameca splendens (Goodeidae) Lombardi and Wourms, 1985b* Trophotaenial placenta Ameca splendens (Goodeidae) Lombardi and Wourms, 1988 Placental function, matrotrophy Ameca splendens (Goodeidae) Meisner and Burns, 1997 Specializations for matrotrophy Hemiramphidae Mendoza, 1937 Trophotaenial resorption Goodeidae Mendoza, 1956 Trophotaeniae and ovary Hubbsina turneri (Goodeidae) Mendoza, 1958 Specializations for matrotrophy Goodea luitpoldii (Goodeidae) Mendoza, 1972 Trophotaeniae Xenotoca eiseni (Goodeidae) Parenti et al, 2010 Reproductive histology Tomeurus gracilis (Poeciliidae) Schindler and de Vries, 1986 Trophotaeniae Girardinichthys viviparus (Goodeidae) Schindler and de Vries, 1988a Specializations for matrotrophy Jenynsia lineata (Anablepidae) Turner, 1933a Viviparity Goodeidae Turner, 1936 Trophotaeniae Parabrotula dentiens (Brotulidae) Turner, 1937 Trophotaeniae Goodeidae Turner, 1938a Ovarian viviparity, matrotrophy Cymatogaster aggregatus (Embiotocidae) Turner, 1938b Specializations for matrotrophy Anableps anableps Turner, 1940a Specializations for matrotrophy Jenynsia (Anablepidae) Turner, 1940b Specializations for matrotrophy Anablepidae Turner, 1940c Specializations for matrotrophy Poeciliidae Turner, 1940d Specializations for matrot...…”

Copulation in antiarch placoderms and the origin of gnathostome internal fertilization

“…Among living fish (non-tetrapod vertebrates) internal fertilization is mostly effected by copulatory structures representing modifications of the pelvic fins (chondrichthyans 9 ) or anal fins (the gonopodium of some teleost fishes 10,11 ). The discovery in arthrodiran 3 and ptyctodont placoderms 2,4 of copulatory structures (claspers) originally 3, 12 but incorrectly 4 interpreted as modified pelvic fins implied that any placoderms lacking pelvic appendages would have also lacked claspers, and therefore reproduced externally by spawning.…”

“…The implied loss of bony claspers and implied reversion to external fertilisation in crown gnathostomes appears heterodox: loss of internal fertilization and acquisition of external fertilization is not widely accepted, at least in vertebrates 1,11 although it could have happened multiple times in invertebrates 24 . The shared, unique morphology and post-pelvic position of claspers in all placoderms is more consistent with a single origin, and thus represents a potential synapomorphy supporting placoderm monophyly 25 .…”