The evolution of euhermaphroditism in caridean shrimps: a molecular perspective of sexual systems and systematics

Abstract

BackgroundThe hippolytid genus Lysmata is characterized by simultaneous hermaphroditism, a very rare sexual system among Decapoda. Specialized cleaning behavior is reported in a few pair-living species; these life history traits vary within the genus. Unfortunately, the systematics of Lysmata and the Hippolytidae itself are in contention, making it difficult to examine these taxa for trends in life history traits. A phylogeny of Lysmata and related taxa is needed, to clarify their evolutionary relationships and the origin of their unique sexual pattern. In this study, we present a molecular phylogenetic analysis among species of Lysmata, related genera, and several putative hippolytids. The analysis is based upon DNA sequences of two genes, 16S mtDNA and nuclear 28S rRNA. Phylogenetic trees were estimated using Bayesian Inference, Maximum Likelihood, and Maximum Parsimony.ResultsPhylogenetic analysis of 29 species of Lysmata, eight genera of Hippolytidae and two genera of Barbouriidae based on a single (16S, 28S) and combined gene approach (16S+28S) indicates that three groups of Lysmata differentiate according to antennular morphology: (1) Lysmata, having a multi-segmented accessory branch, (2) Hippolysmata (prior to Chace 1972), with a one-segmented accessory branch, and (3) a third group of Lysmata outliers, with one-segmented unguiform accessory branch, and close affinity to the genera Exhippolysmata and Lysmatella. The monophyly of the clade bearing a multi-segmented accessory branch is robust. Within the short accessory branch clade, species with specialized cleaning behaviors form a monophyletic clade, however, the integrity of the clade was sensitive to alignment criteria. Other hippolytid and barbouriid genera used in the analysis are basal to these three groups, including one displaying simultaneous hermaphroditism (Parhippolyte). The two barbouriid species occur in a separate clade, but among hippolytid taxa.ConclusionsThe data support the historical morphological division of Lysmata into clades based on accessory branch morphology. The position of the "cleaner" shrimps, indicates that specialized cleaning behavior is a derived trait. The topologies of the cladograms support the monophyly of the barbouriids, but do not support their elevation to familial status. Taxa ancestral to the genus Lysmata display simultaneous hermaphroditism, suggesting that this life history trait evolved outside the genus Lysmata.

Shedding light on the larval genus Eretmocaris: morphological larval features of two closely related trans-isthmian Lysmata species (Decapoda: Caridea: Hippolytidae) described on the basis of laboratory cultured material

“…The tree topology obtained by Baeza (2010) recognizes three of the main subclades previously obtained by Baeza et al (2009b), partially supports the separation of species according to the development of the accessory branch of the outer antennular Xagellum into two diVerent genera or subgenera, and shows that the monophyletic clade comprised by species of Lysmata and Exhippolysmata is divided into 4 subclades: the "Tropical American Clade", the "Cleaner Clade", the "Cosmopolitan Clade", and the "Morpho-variable Clade". Fiedler et al (2010) presents the mitochondrial (16S) and the nuclear ribosomal (28S rRNA) phylogeny of the genus, which supports the historical morphological division of Lysmata into three clades, based on the morphology of the antennular accessory branch: the "Short Accessory Branch clade" or "Hippolysmata Clade", the "Long Accessory Branch clade" or "Lysmata Clade" and the "Unguiform Branch clade". Lysmata moorei (Rathbun, 1901) and L. galapagensis Schmitt, 1924 are two closely related species occurring on the eastern and western sides of the Panama Isthmus, respectively.…”

“…Despite their similarity to L. galapagensis, larvae of L. moorei lack the unique morphological feature displayed by L. galapagensis on the third pleomere. Regardless of the close phylogenetic relationship suggested by the molecular studies by Baeza et al (2009b), Baeza (2010) and Fiedler et al (2010) between the eastern PaciWc L. galapagensis and the western Atlantic L. moorei. The most evident larval character shared by the eastern PaciWc L. galapagensis and the western Atlantic L. moorei is the presence of a very long rostrum with several teeth in late zoeal stages.…”

“…The molecular phylogeny of Lysmata has been recently studied by several authors (Baeza et al 2009b;Baeza 2010;Fiedler et al 2010). Baeza et al (2009b) and Baeza (2010) presented the molecular phylogeny of the genus based on a segment of the 16S rRNA mitochondrial DNA.…”

“…Lysmata moorei (Rathbun, 1901) and L. galapagensis Schmitt, 1924 are two closely related species occurring on the eastern and western sides of the Panama Isthmus, respectively. The two species are considered sister taxa, included in the monophyletic "Long Branch Clade" (Fiedler et al 2010). …”

Confirmation of the presence of Janicea antiguensis (Chace, 1972) (Decapoda: Barbouriidae) in northeastern and eastern Brazil

“…This type of hermaphroditism has been demonstrated in at least one other barbouriid shrimp, Parhippolyte misticia (Onaga et al, 2012), and in a number of species of the more distantly related hippolytid genera Lysmata Risso, 1816and Exhippolysmata Stebbing, 1916(Bauer and Holt, 1998Bauer, 2000;Baeza and Bauer, 2004;Baeza, 2006;Braga et al, 2009;Fiedler et al, 2010). The morphological and anatomical details of the presumed hermaphroditism in J. antiguensis remain to be investigated.…”