Patterns of population genetic structure and connectivity of squat lobsters associated with vulnerable marine ecosystems

<p>Vulnerable marine ecosystems (VMEs) are susceptible to the impact of intense or long-term anthropogenic activities (e.g., bottom trawling). Networks of marine protected areas (MPAs) can help facilitate the conservation and restoration of biodiversity and ecosystem function provided by VMEs. An understanding of the connectivity amongst populations of deep-sea organisms is crucial for informing the management of VMEs, by assessing the effectiveness of existing MPAs and informing the placement of new MPAs. Genetic evaluation of population structure is one of the most commonly used indirect approaches for interpreting connectivity. In contrast to corals or sponges, which are typically habitat-forming organisms as VME-indicator taxa, squat lobsters are often found in close association with VMEs and can be considered to be VME-associated taxa. Nowadays, population genetic studies of deep-sea fauna mainly focus on VME-indicator taxa, whilst relatively few studies have focussed on VME-associated taxa, such as squat lobsters, whose distribution is not exclusively limited to VMEs. In this study, three deep-sea squat lobster species, Munida isos Ahyong & Poore, 2004, Munida endeavourae Ahyong & Poore, 2004 and Munida gracilis Henderson, 1885, were selected based on their association with VMEs (e.g., cold-water coral reefs and seamounts), wide distributional ranges across the southwest Pacific Ocean, and sample availability. The overall aims of this research are to evaluate patterns of population structure and genetic connectivity of three squat lobster taxa in the southwest Pacific Ocean and consider how the acquired genetic information can contribute to the management and conservation of VMEs in the southwest Pacific Ocean. A general introduction of VMEs, MPAs, connectivity of deep-sea fauna, High-Throughput Sequencing (HTS), study area and study taxa are presented in Chapter 1. To provide background information for this research, a review was conducted of the molecular-based studies of the systematics, taxonomy and phylogenetics of marine squat lobster taxa (Chapter 2). Recent molecular-based studies have dramatically increased our understanding of squat lobster phylogenetics and systematics, and thereby the taxonomy of this diverse and challenging group, which provide a valuable starting point for evaluating hypotheses concerning speciation, biogeography, adaptation and co-evolution (e.g., squat lobsters and corals). Notably, accurate taxonomy is critical for population genetic studies and consequently supports the conservation efforts of VMEs. A range of molecular genetic markers, including the mitochondrial COI region, nuclear microsatellites and single nucleotide polymorphisms (SNPs), were utilised to evaluate the genetic connectivity amongst populations of three VME-associated taxa (Munida isos, M. endeavourae and M. gracilis). In addition to this, universal invertebrate primers were used to yield partial COI fragments of 649 bp (DNA barcoding) for the three Munida species to confirm the taxonomic identity and to exclude the possibility of cryptic species. Due to limited genetic information for the three Munida species, novel microsatellite loci were developed for M. isos based on the HiSeq 2500 sequencing platform and used for cross-species amplification in M. endeavourae and M. gracilis (Chapter 3). Additionally, a Genotyping by Sequencing (GBS) protocol and the Universal Network Enabled Analysis Kit (UNEAK) pipeline were employed to develop novel SNPs for M. isos samples from the southwest Pacific Ocean (Chapter 5). A spatially explicit hierarchical testing framework (Northern-Southern biogeographical provinces, North-Central-South regions, and individual geomorphic features) was employed for the evaluation of connectivity amongst populations of the three deep-sea squat lobster taxa across their distributional range in the southwest Pacific Ocean (Chapter 4). The level of genetic diversity was high as revealed by variation at the COI region, and moderate based on microsatellite markers across the three Munida species. With more than 96% of the variance being attributed to differences within populations in the three Munida species, based on both marker types, no genetic subdivision was detected in M. endeavourae, whilst little genetic differentiation was observed in M. isos and M. gracilis based on microsatellite variation. For M. isos, populations from the Tasmanian slope were potentially genetically different from all other populations and may act as source populations, whereas populations from the Kermadec Ridge may be sink populations. Robust evidence of recent demographic expansions was detected in the three Munida species, based on COI and microsatellite marker types. The estimated time of demographic expansions for the three Munida species was ca. 16.1 kya, 24.4 kya and 21.6 kya for the M. isos, M. endeavourae and M. gracilis, respectively, coinciding with the late Pleistocene. The results are discussed in the context of the distribution of existing MPAs, and contribute new information useful to the management of VMEs within national and international waters in the region. To further investigate patterns of connectivity in deep-sea squat lobster populations and provide valuable information for the design of management strategies to protect VMEs, newly developed SNPs were utilised (Chapter 5). The results showed that the Tasmanian slope and Macquarie Ridge populations were genetically different from all other populations, both within New Zealand’s exclusive economic zone (EEZ) and the high seas beyond, with little gene flow derived from Tasmanian slope populations to Macquarie Ridge populations. The results are discussed in the context of existing MPAs, and highlight the complexity of the endeavour to maintain population diversity and gene flow across multiple national jurisdictions as well as international waters, all of which employ different spatial protective measures. The findings of this research are summarised and discussed in relation to the usefulness of genetic studies to provide new and valuable information about the genetic diversity and connectivity of VME-associated species, and to highlight what additional genetic research is needed to assist in the management and conservation of VMEs in the southwest Pacific Ocean (Chapter 6).</p>

Patterns of population genetic structure and connectivity of squat lobsters associated with vulnerable marine ecosystems

<p>Vulnerable marine ecosystems (VMEs) are susceptible to the impact of intense or long-term anthropogenic activities (e.g., bottom trawling). Networks of marine protected areas (MPAs) can help facilitate the conservation and restoration of biodiversity and ecosystem function provided by VMEs. An understanding of the connectivity amongst populations of deep-sea organisms is crucial for informing the management of VMEs, by assessing the effectiveness of existing MPAs and informing the placement of new MPAs. Genetic evaluation of population structure is one of the most commonly used indirect approaches for interpreting connectivity. In contrast to corals or sponges, which are typically habitat-forming organisms as VME-indicator taxa, squat lobsters are often found in close association with VMEs and can be considered to be VME-associated taxa. Nowadays, population genetic studies of deep-sea fauna mainly focus on VME-indicator taxa, whilst relatively few studies have focussed on VME-associated taxa, such as squat lobsters, whose distribution is not exclusively limited to VMEs. In this study, three deep-sea squat lobster species, Munida isos Ahyong & Poore, 2004, Munida endeavourae Ahyong & Poore, 2004 and Munida gracilis Henderson, 1885, were selected based on their association with VMEs (e.g., cold-water coral reefs and seamounts), wide distributional ranges across the southwest Pacific Ocean, and sample availability. The overall aims of this research are to evaluate patterns of population structure and genetic connectivity of three squat lobster taxa in the southwest Pacific Ocean and consider how the acquired genetic information can contribute to the management and conservation of VMEs in the southwest Pacific Ocean. A general introduction of VMEs, MPAs, connectivity of deep-sea fauna, High-Throughput Sequencing (HTS), study area and study taxa are presented in Chapter 1. To provide background information for this research, a review was conducted of the molecular-based studies of the systematics, taxonomy and phylogenetics of marine squat lobster taxa (Chapter 2). Recent molecular-based studies have dramatically increased our understanding of squat lobster phylogenetics and systematics, and thereby the taxonomy of this diverse and challenging group, which provide a valuable starting point for evaluating hypotheses concerning speciation, biogeography, adaptation and co-evolution (e.g., squat lobsters and corals). Notably, accurate taxonomy is critical for population genetic studies and consequently supports the conservation efforts of VMEs. A range of molecular genetic markers, including the mitochondrial COI region, nuclear microsatellites and single nucleotide polymorphisms (SNPs), were utilised to evaluate the genetic connectivity amongst populations of three VME-associated taxa (Munida isos, M. endeavourae and M. gracilis). In addition to this, universal invertebrate primers were used to yield partial COI fragments of 649 bp (DNA barcoding) for the three Munida species to confirm the taxonomic identity and to exclude the possibility of cryptic species. Due to limited genetic information for the three Munida species, novel microsatellite loci were developed for M. isos based on the HiSeq 2500 sequencing platform and used for cross-species amplification in M. endeavourae and M. gracilis (Chapter 3). Additionally, a Genotyping by Sequencing (GBS) protocol and the Universal Network Enabled Analysis Kit (UNEAK) pipeline were employed to develop novel SNPs for M. isos samples from the southwest Pacific Ocean (Chapter 5). A spatially explicit hierarchical testing framework (Northern-Southern biogeographical provinces, North-Central-South regions, and individual geomorphic features) was employed for the evaluation of connectivity amongst populations of the three deep-sea squat lobster taxa across their distributional range in the southwest Pacific Ocean (Chapter 4). The level of genetic diversity was high as revealed by variation at the COI region, and moderate based on microsatellite markers across the three Munida species. With more than 96% of the variance being attributed to differences within populations in the three Munida species, based on both marker types, no genetic subdivision was detected in M. endeavourae, whilst little genetic differentiation was observed in M. isos and M. gracilis based on microsatellite variation. For M. isos, populations from the Tasmanian slope were potentially genetically different from all other populations and may act as source populations, whereas populations from the Kermadec Ridge may be sink populations. Robust evidence of recent demographic expansions was detected in the three Munida species, based on COI and microsatellite marker types. The estimated time of demographic expansions for the three Munida species was ca. 16.1 kya, 24.4 kya and 21.6 kya for the M. isos, M. endeavourae and M. gracilis, respectively, coinciding with the late Pleistocene. The results are discussed in the context of the distribution of existing MPAs, and contribute new information useful to the management of VMEs within national and international waters in the region. To further investigate patterns of connectivity in deep-sea squat lobster populations and provide valuable information for the design of management strategies to protect VMEs, newly developed SNPs were utilised (Chapter 5). The results showed that the Tasmanian slope and Macquarie Ridge populations were genetically different from all other populations, both within New Zealand’s exclusive economic zone (EEZ) and the high seas beyond, with little gene flow derived from Tasmanian slope populations to Macquarie Ridge populations. The results are discussed in the context of existing MPAs, and highlight the complexity of the endeavour to maintain population diversity and gene flow across multiple national jurisdictions as well as international waters, all of which employ different spatial protective measures. The findings of this research are summarised and discussed in relation to the usefulness of genetic studies to provide new and valuable information about the genetic diversity and connectivity of VME-associated species, and to highlight what additional genetic research is needed to assist in the management and conservation of VMEs in the southwest Pacific Ocean (Chapter 6).</p>

A new species of Pseudione sensu lato (Isopoda: Bopyridae) on a squat lobster host from the deep South-West Atlantic

A new bopyrid, Pseudione chiesai n. sp., is herein described based on an ovigerous female and an adult male found in the right branchial chamber on a specimen of Munida spinosa Henderson, 1885. This parasite was collected in the Mar del Plata submarine canyon at 819 m depth during the expedition “Talud Continental I” carried out by the Argentine RV Puerto Deseado in 2012. P. chiesai n. sp. belongs to the Pseudione “crénelés” group sensu Bourdon (1972, 1976), which currently contains seven species, all of which have galatheoid crabs as hosts. P. chiesai n. sp. can be separated from the other species in the Pseudione “crénelés” group by the following combination of characters: (1) both sides of the body convex, (2) frontal lamina with a few, shallow indentations, (3) coxal plates 1–4 and tergal projections 1–4 with distinct irregular margins, mainly on the right side, (4) pereomeres 5–7 with single/branched lateral digitations, (5) maxilliped palp well-developed and setose, and (6) pleon with lateral plates 1–5 distally rounded and directed laterally. The taxonomic position of this new species is briefly discussed.

Separate Feeding Between the Pelagic Stage of the Squat Lobster Munida gregaria and the Larger Sized Zooplankton Crustacean Groups in the Beagle Channel as Revealed by Stable Isotopes

In southern Patagonia, the Beagle Channel shows very low production during winter but simultaneously sustains very dense aggregations of the pelagic stage of squat lobster (Munida gregaria), a benthic decapod whose pelagic juveniles have the largest body size within the chitinous pelagic community. To assess the coexistence of the mesozooplankton community and the pelagic M. gregaria stage under the harsh feeding winter conditions, we conducted a research cruise at two locations connected to the Beagle Channel, Yendegaia Bay (land terminating-glacier) and Pia Fjord (marine-terminating glacier). Our results showed that the zooplankton communities were similar in these two fjords, that a single pelagic group dominated in terms of biomass (pelagic Munida gregaria), and that differences in vertical distribution existed between most of the principal crustacean zooplankton and pelagic M. gregaria. All groups showed consumption of terrestrially derived organic matter, as revealed by their δ13C values. However, the isotopic composition, trophic positions (TP), and isotopic niche areas of the groups separated pelagic M. gregaria, presenting some of the lowest δ15N and the highest δ13C values, and the narrowest isotopic niche width. Pelagic M. gregaria was dominated by a single body size class along the 0–100 m water column, with no diel changes in vertical distribution, remained mostly in the upper layers (0–50 m), and benefited from the slightly higher phytoplankton concentrations at shallower depths as revealed by their higher δ13C values and low trophic position. In contrast, the other groups, including zoea M. gregaria stages, developed changes in distribution between day and night or remained deeper in the water column. These groups showed higher δ15N values, higher TP, and lower δ13C values, most of which probably fed on a nanoheterotrophs and terrestrial particulate organic matter mixture at deeper layers. Thus, the different vertical distributions, different trophic level food sources, and slightly different organic carbon sources apparently reduced any potential competence for food resources and form part of the feeding strategy that may facilitate the coexistence of the different large pelagic crustaceans under harsh feeding winter conditions in this high latitude austral region.

A new species of the squat lobster genus Uroptychodes Baba, 2004 (Decapoda: Anomura: Chirostylidae) from Japan

A new species of the chirostylid squat lobster genus Uroptychodes Baba, 2004, U. fuscilineatus, is described and illustrated on the basis of a single ovigerous female from the Uraga Channel, central Japan, at depth of 250 m. The new species appears most similar to U. spinimarginatus (Henderson, 1885) and U. yapensis Dong, Gan & Li, 2021 among the 13 known congeners, but is notable in the pereopod 2 not being definitely more slender than the pereopods 3 and 4 and the remarkably spinose pereopods 1–4. A possible association of the new species with crinoid is suggested. An updated identification key to species of Uroptychodes is presented.

Dirivultidae (Copepoda: Siphonostomatoida) from hydrothermal vent fields in the Okinawa Trough, North Pacific Ocean, with description of one new species

Two species of dirivultid copepod (Siphonostomatoida), Stygiopontius senckenbergi Ivanenko & Ferrari, 2013 and Dirivultus kaiko sp. nov., were discovered from hydrothermal vent fields in the Okinawa Trough, the western North Pacific. Since S. senckenbergi was originally described based on two adult males from the New Ireland Fore-Arc system, Papua New Guinea, the discovery here represents the second record. This species was attached on ventral setae covered with filamentous bacteria of the deep-sea squat lobster Shinkaia crosnieri (Decapoda: Munidopsidae). The female of S. senckenbergi is described for the first time as well as the nauplius I and the copepodid IV. Sexual dimorphism is shown on several appendages (i.e. antennule, leg 2 and leg 5). The nauplius I shows typical lethithotrophic characteristics. Dirivultus kaiko sp. nov., which was found on the tentacular crown of the siboglinid tubeworm Lamellibrachia columna, differs from its two congeners by the antennule, maxilliped and leg 5 of both sexes. These are the second and third dirivultid species to be reported from Japan.

A new species and depth record of bopyrid (Crustacea, Isopoda) from a squat lobster in the Kuril-Kamchatka Trench

The branchial parasitic isopod Pleurocryptella altalis sp. nov. (Bopyridae: Pseudioninae) is described from the squat lobster host Munidopsis petalorhyncha Baba, 2005. The new species is morphologically similar to Pleurocryptella formosa Bonnier, 1900 and P. wolffi Bourdon, 1972b but can be distinguished based on male characters (differences in head, pleon and uropods) and female characters (differences in barbula, pleopods and pleotelson). The parasite specimens (a female and male pair) were collected with the squat lobster host at a depth of 5060–5130 m from the Kuril-Kamchatka Trench, representing the deepest record for any of the 850+ described bopyrid isopod species and for any record of an infested host. Dichotomous identification keys to females and males of Pleurocryptella species and subspecies are provided.