Out of Asia: mitochondrial evolutionary history of the globally introduced supralittoral isopodLigia exotica

Abstract

The native ranges and invasion histories of many marine species remain elusive due to a dynamic dispersal process via marine vessels. Molecular markers can aid in identification of native ranges and elucidation of the introduction and establishment process. The supralittoral isopod Ligia exotica has a wide tropical and subtropical distribution, frequently found in harbors and ports around the globe. This isopod is hypothesized to have an Old World origin, from where it was unintentionally introduced to other regions via wooden ships and solid ballast. Its native range, however, remains uncertain. Recent molecular studies uncovered the presence of two highly divergent lineages of L. exotica in East Asia, and suggest this region is a source of nonindigenous populations. In this study, we conducted phylogenetic analyses (Maximum Likelihood and Bayesian) of a fragment of the mitochondrial 16S ribosomal (r)DNA gene using a dataset of this isopod that greatly expanded previous representation from Asia and putative nonindigenous populations around the world. For a subset of samples, sequences of 12S rDNA and NaK were also obtained and analyzed together with 16S rDNA. Our results show that L. exotica is comprised of several highly divergent genetic lineages, which probably represent different species. Most of the 16S rDNA genetic diversity (48 haplotypes) was detected in East and Southeast Asia. Only seven haplotypes were observed outside this region (in the Americas, Hawai’i, Africa and India), which were identical or closely related to haplotypes found in East and Southeast Asia. Phylogenetic patterns indicate the L. exotica clade originated and diversified in East and Southeast Asia, and only members of one of the divergent lineages have spread out of this region, recently, suggesting the potential to become invasive is phylogenetically constrained.

Molecular approaches uncover cryptic diversity in intertidalLigiaisopods (Crustacea, Isopoda, Ligiidae) across the southern Africa coastline

“…By using morphological identifications as well as nuclear and mitochondrial markers to characterize 18 Ligia populations from southern Africa, we report patterns that suggest the biodiversity of these isopods is under-reported in this region. Our findings are in line with reports of allopatric genetic differentiation across Ligia species from other regions ( Eberl et al, 2013 ; Hurtado, Mateos & Santamaria, 2010 ; Hurtado et al, 2018 ; Raupach et al, 2014 ; Santamaria et al, 2017 ; Santamaria, Mateos & Hurtado, 2014 ; Santamaria et al, 2013 ; Taiti et al, 2003 ; Yin et al, 2013 ), as well as reports of cryptic diversity within other coastal invertebrates along the coastline of South Africa ( Baldanzi et al, 2016 ; Evans et al, 2004 ; Ridgway et al, 2001 ; Teske et al, 2006 ; Teske et al, 2007 ; Zardi et al, 2007 ). The presence of several cryptic lineages within nominal Ligia species in southern Africa suggest the possible presence of putative cryptic species in the area, underscoring the need of taxonomic evaluation to determine whether these lineages are indeed valid species.…”

“…Adult Ligia isopods avoid open water and quickly attempt to regain the shore when submerged ( Barnes, 1932 ; Barnes, 1935 ), exhibit low desiccation and submergence resistance ( Barnes, 1936 ; Barnes, 1938 ; Todd, 1963 ; Tsai, Dai & Chen, 1997 ; Tsai, Dai & Chen, 1998 ; Zhang et al, 2016 ) and poor locomotion on non-rocky substrates. These traits limit both their overland and overwater dispersal potential, which may lead to severely restricted gene flow between populations, long term isolation, and in turn allopatric and potentially cryptic diversification, as reported for L. hawaiensis ( Santamaria et al, 2013 ; Taiti et al, 2003 ), L. exotica and L. cinerascens ( Hurtado et al, 2018 ; Yin et al, 2013 ), L. occidentalis ( Hurtado, Mateos & Santamaria, 2010 ), L. baudiniana ( Santamaria, Mateos & Hurtado, 2014 ), L. oceanica ( Raupach et al, 2014 ), as well L. vitiensis and L. dentipes ( Santamaria et al, 2017 ). Thus, molecular characterization of yet to be studied Ligia species may also uncover evidence suggestive of cryptic diversification.…”

A Framework for Understanding Marine Cosmopolitanism in the Anthropocene

“…The hypothesis that these clades represent multiple species is supported by extraordinary genetic divergence, comparable with inter-specific distances observed in other colonial ascidians. Similar patterns of cosmopolitan “species” comprising provincial genetic lineages have been observed in isopods (Hurtado et al, 2018), polychaetes (Sun et al, 2017), and multiple hydrozoans (Miglietta et al, 2015; Govindarajan et al, 2017). In the absence of formal taxonomic revision, all of these species appear based on genetic evidence to harbor multiple lineages—possibly themselves all distinct species—that are most decidedly not cosmopolitan.…”

“…However, often one or more novel lineages retains a cosmopolitan distribution, and the question then turns to the nature of that distribution, and whether it has been influenced by anthropogenic dispersal. As we have already noted, D. listerianum Clade A appears to be a globally distributed independent evolutionary lineage; similarly, Clade A of the polychaete Hydroides dianthus has been found in the northwest and southwest Atlantic, Mediterranean, and western Pacific (Sun et al, 2017); and Clade D of the isopod Ligia exotica may be native to East Asia but has been identified from South Africa, India, the western Atlantic, and Hawaii (Hurtado et al, 2018). In all cases, molecular genetic as well as historical evidence support the hypothesis that these clades represent as-yet unnamed neocosmopolitan species.…”

Molecular taxonomy of endemic coastalLigiaisopods from the Hawaiian Islands: re-description ofL. hawaiensisand description of seven novel cryptic species

“…Such low vagility and the patchiness of Ligia habitats (i.e., rocky intertidal coastlines) have been suggested to restrict gene flow, leading to long-term isolation and deep genetic divergence between populations even across small geographic distances (e.g., Jung et al, 2008; Hurtado, Mateos & Santamaria, 2010; Eberl et al, 2013; Santamaria et al, 2013). Not surprisingly, molecular characterizations have uncovered highly divergent genetic lineages in several Ligia species around the world suggesting that some species may represent cryptic species complexes in need of formal taxonomic description (Jung et al, 2008; Hurtado, Mateos & Santamaria, 2010; Santamaria et al, 2013; Raupach et al, 2014; Santamaria, Mateos & Hurtado, 2014; Santamaria et al, 2017; Greenan, Griffiths & Santamaria, 2018; Hurtado et al, 2018). One such example is that of Ligia from the coastlines of the Hawaiian archipelago.…”