Systematics and Reproductive Evolution in the Family Characidae (Teleostei: Ostariophysi) Open Access
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Internal fertilization and its necessary precursor, insemination, are uncommon among teleost fishes. External fertilization, in contrast, is the reproductive mode for the vast majority (97%) of teleost fishes. Histological studies indicate that more than 60 species in the family Characidae are inseminating. Most of these inseminating characids are part of the lineage that has been recently diagnosed by characters of the upper jaw dentition and dorsal fin--the so-called "clade A." The null hypothesis for evolution of insemination in the Characidae is that it evolved once and all species exhibiting this reproductive mode are more closely related to one another than they are to other characids. The alternative hypothesis is that insemination has multiple origins in the family and that not all instances of insemination are homologous across the family. To reject the null hypothesis it was necessary to consider the phylogeny of the Characidae. Molecular sequence data were collected from four gene fragments (12S, 16S, COI, and RAG2). The first three genes are part of the mitochondrial genome, whereas the latter is part of the nuclear genome. These genes were chosen, in part, because data from these genes in characid fishes have been published by previous authors and it was therefore possible to combine them with newly acquired sequences. Statements of positional homology were created using the sequence-alignment program MAFFT. Equal-weights parsimony and stochastic models of nucleotide substitution were then used for phylogenetic inference with parsimony and Bayesian methods, respectively. Trees were rooted with Chalceus macrolepidotus, a species considered basal in either the Characidae or, more recently, the Alestidae. Great variability was exhibited in nodal support, as estimated with Bremer support values and bootstrap values in the parsimony analysis and posterior probabilities in Bayesian analysis. The monophyly of clade A was not rejected, but the following taxa were rejected as monophyletic: Hemigrammus, Hyphessobrycon, Astyanax, Bryconamericus, and subfamily Stevardiinae. Sister-group relationships were inferred for the following pairs of taxa: Acestrorhynchus and Bryconops, Brittanichthys and Paracheirodon, Hollandichthys and Rachoviscus, Mimagoniates and tribe Corynopomini, Tetragonopterinae and Characinae (excluding Gnathocharax), and Aphyocharacinae and Cheirodontinae. When the reproductive mode of insemination is optimized onto either the strict consensus cladogram from the parsimony analysis or the Bayesian phylogram, it has at least four origins: at least one origin in clade A, at least one origin among cheirodontines, and two origins among the "clade C" characids: one in the lineage represented by Brittanichthys axelrodi and the other in the Hollandichthys plus Rachoviscus clade. Thus, the hypothesis of a single origin of insemination among characid fishes is rejected. Certain reproductive characters are closely associated with evolutionary shifts between external fertilization and insemination. Though the following characters are not prerequisites for insemination per se, when any is present in a characid species, that species is also inseminating: large aspermatogenic storage region in testis, production of spermatozeugmata, elongate sperm nuclei, striated rootlet in spermatozoon, large overlap of mitochondria and posterior portion of sperm nucleus, accessory microtubules in spermatozoon, and electron-dense A-tubules of axoneme in spermatozoon. This research involved discovery of insemination and the male secondary sex character known as the "gill gland" in species not previously known to exhibit either trait. If the gill gland evolved only once (and were subsequently lost in some descendant clades), then insemination is far more heavily concentrated in the lineage descended from this ancestor (clades A + B) than it is in the sister lineage (clade C). The elongate structures displayed during courtship rituals of corynopomin fishes may exemplify behavioral homology with substitution of morphological substrates.
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