Molecular phylogenetic analysis of the Paguristes tortugae Schmitt, 1933 complex and selected other Paguroidea (Crustacea: Decapoda: Anomura)

Abstract

Morphological characters, as presently applied to describe members of the Paguristes tortugae Schmitt, 1933 species complex, appear to be of limited value in inferring phylogenetic relationships within the genus, and may have similarly misinformed understanding of relationships between members of this complex and those presently assigned to the related genera Areopaguristes Rahayu & McLaughlin, 2010 and Pseudopaguristes McLaughlin, 2002. Previously undocumented observations of similarities and differences in color patterns among populations additionally suggest genetic divergences within some species, or alternatively seem to support phylogenetic groupings of some species. In the present study, a Maximum Likelihood (ML) phylogenetic analysis was undertaken based on the H3, 12S mtDNA, and 16S mtDNA sequences of 148 individuals, primarily representatives of paguroid species from the western Atlantic. This molecular analysis supported a polyphyletic Diogenidae Ortmann, 1892, although incomplete taxonomic sampling among the genera of Diogenidae limits the utility of this finding for resolving family level relationships. Several hypotheses regarding the evolutionary relationships among hermit crab genera were refuted by the Kishino-Hasegawa (KH). Shimodaira-Hasegawa (SH) and Approximately Unbiased (AU) tree topology tests, among them the hypothesis that Areopaguristes is monophyletic. A lack of support for the monophyly of Areopaguristes calls into question the phylogenetic validity of gill number for the differentiation of Paguristes, Areopaguristes, and Pseudopaguristes. The study was inconclusive with regard to the relationships among these three genera, but previously unknown diversity within both Paguristes and Areopaguristes was demonstrated. Existence of an undescribed species confounded under the name Paguristes tortugae Schmitt, 1933 was supported by genetics, morphology, and coloration. A second undescribed species with remarkable similarity to Areopaguristes hummi Wass, 1955 was discovered based on genetics and coloration.

Two new marine hermit crabs allied with the Paguristes tortugae complex (Crustacea: Decapoda: Anomura) from the western Atlantic

“…Diogenidae Ortmann, 1892 has historically been treated as a monophyletic family (e.g., MacDonald et al 1957;McLaughlin 1983McLaughlin , 2002Cunningham et al 1992;McLaughlin & Lemaitre 1997;Forest & McLaughlin 2000;Ahyong & O'Meally 2004;McLaughlin et al 2007McLaughlin et al , 2010Ahyong et al 2009;De Grave et al 2009), whereas others argued against this hypothesis (Tudge 1995(Tudge , 1997Tsang et al 2008Tsang et al , 2011Bybee et al 2011;Schnabel et al 2011;Bracken-Grissom et al 2013;Gong et al 2018;Landschoff & Gouws 2018;Tan et al 2018;Wolfe et al 2019). Craig & Felder (2021) presented further molecular evidence against diogenid monophyly and identified three major genetic clades. One of these monophyletic subgroups, Diogenidae Clade 1, included all Paguristes Dana, 1851, Areopaguristes Rahayu &Pseudopaguristes McLaughlin, 2002. This suggested that Diogenidae Clade 1 represented a multi-generic complex of over 200 species (McLaughlin & Lemaitre 2020;WoRMS 2020).…”

“…One of these monophyletic subgroups, Diogenidae Clade 1, included all Paguristes Dana, 1851, Areopaguristes Rahayu &Pseudopaguristes McLaughlin, 2002. This suggested that Diogenidae Clade 1 represented a multi-generic complex of over 200 species (McLaughlin & Lemaitre 2020;WoRMS 2020). The three constituent genera of Diogenidae Clade 1 were once thought to be readily differentiated from each other by gill-pair number (McLaughlin 2002;Forest et al 2000;Rahayu 2005, but findings of previous molecular phylogenetic analyses indicated that gill-pair number was not evolutionarily conserved within any of the three genera (Bracken-Grissom et al 2013;Craig & Felder 2021). Molecular findings continue to support generally close alliance of the three genera, but the precise evolutionary relationships the generic level have remained unresolved (Bracken-Grissom et al 2013;Landschoff & Gouws 2018;Craig & Felder 2021).…”

“…The three constituent genera of Diogenidae Clade 1 were once thought to be readily differentiated from each other by gill-pair number (McLaughlin 2002;Forest et al 2000;Rahayu 2005, but findings of previous molecular phylogenetic analyses indicated that gill-pair number was not evolutionarily conserved within any of the three genera (Bracken-Grissom et al 2013;Craig & Felder 2021). Molecular findings continue to support generally close alliance of the three genera, but the precise evolutionary relationships the generic level have remained unresolved (Bracken-Grissom et al 2013;Landschoff & Gouws 2018;Craig & Felder 2021). Despite substantial uncertainty surrounding diogenid relationships at the levels of family and genus, some historically recognized species-level morphogroups roughly correlated with clades within Diogenidae Clade 1 in recent molecular phylogenetic analyses (Bracken-Grissom et al 2013;Craig & Felder 2021).…”

“…Molecular findings continue to support generally close alliance of the three genera, but the precise evolutionary relationships the generic level have remained unresolved (Bracken-Grissom et al 2013;Landschoff & Gouws 2018;Craig & Felder 2021). Despite substantial uncertainty surrounding diogenid relationships at the levels of family and genus, some historically recognized species-level morphogroups roughly correlated with clades within Diogenidae Clade 1 in recent molecular phylogenetic analyses (Bracken-Grissom et al 2013;Craig & Felder 2021). One of these morphogroups, the Paguristes tortugae complex, originally included many western Atlantic species of Paguristes, several of which have been tranferred to Areopaguristes or Pseudopaguristes.…”

“…Four of these, Paguristes maclaughlinae Martinez-Iglesias & Sanchez, 1989, P. werdingi Campos & Sanchez, 1995, P. zebra Campos & Sanchez, 1995, and P. scarabinoi Lima & Santana, 2017, were assigned to the complex at the time of their descriptions, based primarily on the characteristic pattern of setation. Phylogenetic analysis of available genetic data in some cases suggested the inclusion of Areopaguristes tudgei (Bracken-Grissom et al 2013Craig & Felder 2021) and A. hummi (Wass, 1955) (Bracken-Grissom et al 2013), although morphological arguments for these assignments were not conclusive . With these additions, the P. tortugae complex now spans a broad geographic distribution throughout the western Atlantic (Felder et al 2009;Lemaitre & Tavares 2015), with constituent species found across multiple ecoregions (Spalding et al 2007) from the Carolinean province on the eastern coast of North America, southwards beyond Rio de Janerio, Brazil (Table 1).…”