The little shrimp that could: phylogeography of the circumtropical Stenopus hispidus (Crustacea: Decapoda), reveals divergent Atlantic and Pacific lineages
Title: The little shrimp that could: phylogeography of the circumtropical Stenopus hispidus (Crustacea: Decapoda), reveals divergent Atlantic and Pacific lineages
The banded coral shrimp, Stenopus hispidus (Crustacea: Decapoda: Stenopodidea) is a popular marine ornamental species with a circumtropical distribution. The planktonic larval stage lasts ∼120–253 days, indicating considerable dispersal potential, but few studies have investigated genetic connectivity on a global scale in marine invertebrates. To resolve patterns of divergence and phylogeography of S. hispidus , we surveyed 525 bp of mitochondrial cytochrome c oxidase subunit I (COI) from 198 individuals sampled at 10 locations across ∼27,000 km of the species range. Phylogenetic analyses reveal that S. hispidus has a Western Atlantic lineage and a widely distributed Indo-Pacific lineage, separated by sequence divergence of 2.1%. Genetic diversity is much higher in the Western Atlantic ( h = 0.929; π = 0.004) relative to the Indo-Pacific ( h = 0.105; π < 0.001), and coalescent analyses indicate that the Indo-Pacific population expanded more recently (95% HPD (highest posterior density) = 60,000–400,000 yr) than the Western Atlantic population (95% HPD = 300,000–760,000 yr). Divergence of the Western Atlantic and Pacific lineages is estimated at 710,000–1.8 million years ago, which does not readily align with commonly implicated colonization events between the ocean basins. The estimated age of populations contradicts the prevailing dispersal route for tropical marine biodiversity (Indo-Pacific to Atlantic) with the oldest and most diverse population in the Atlantic, and a recent population expansion with a single common haplotype shared throughout the vast Indian and Pacific oceans. In contrast to the circumtropical fishes, this diminutive reef shrimp challenges our understanding of conventional dispersal capabilities of marine species. more »« less
Titus, Benjamin M.; Daly, Marymegan; Hamilton, Natalie; Berumen, Michael L.; Baeza, J. Antonio(
, Journal of Biogeography)
AbstractAim
The “sexy shrimp”Thor amboinensisis currently considered a single circumtropical species. However, the tropical oceans are partitioned by hard and soft barriers to dispersal, providing ample opportunity for allopatric speciation. Herein, we test the null hypothesis thatT. amboinensisis a single global species, reconstruct its global biogeographical history, and comment on population‐level patterns throughout the Tropical Western Atlantic.
Location
Coral reefs in all tropical oceans.
Methods
Specimens ofThor amboinensiswere obtained through field collection and museum holdings. We used one mitochondrial (COI) and two nuclear (NaK, enolase) gene fragments for global species delimitation and phylogenetic analyses (n = 83 individuals, 30 sample localities), while phylogeographical reconstruction in theTWAwas based onCOIonly (n = 303 individuals, 10 sample localities).
Results
We found evidence for at least five cryptic lineages (9%–22%COIpairwise sequence divergence): four in the Indo‐West Pacific and one in the Tropical Western Atlantic. Phylogenetic reconstruction revealed that endemic lineages from Japan and the South Central Pacific are more closely related to the Tropical Western Atlantic lineage than to a co‐occurring lineage that is widespread throughout the Indo‐West Pacific. Concatenated and species tree phylogenetic analyses differ in the placement of an endemic Red Sea lineage and suggest alternate dispersal pathways into the Atlantic. Phylogeographical reconstruction throughout the Tropical Western Atlantic reveals little genetic structure over more than 3,000 km.
Main conclusions
Thor amboinensisis a species complex that has undergone a series of allopatric speciation events and whose members are in secondary contact in the Indo‐West Pacific. Nuclear‐ and mitochondrial‐ gene phylogenies show evidence of introgression between lineages inferred to have been separated more than 20 Ma. Phylogenetic discordance between multi‐locus analyses suggest thatT. amboinensisoriginated in the Tethys sea and dispersed into the Atlantic and Indo‐West Pacific through the Tethys seaway or, alternatively, originated in the Indo‐West Pacific and dispersed into the Atlantic around South Africa. Population‐level patterns in the Caribbean indicate extensive gene flow across the region.
Xu, T.; Bravo, H.; Paulay, G.; van der Meij, S.E.T.(
, Coral Reefs - this is not a proceedings, it is a journal, but it is not in your dropdown!?)
null
(Ed.)
Coral reefs are home to the greatest diversity of marine life, and many species on reefs live in symbiotic associations. Studying the historical biogeography of symbiotic species is key to unravelling (potential) coevolutionary processes and explaining species richness patterns. Coral-dwelling gall crabs (Cryptochiridae) live in obligate symbiosis with a scleractinian host, and are ideally suited to study the evolutionary history between heterogeneous taxa involved in a symbiotic relationship. The genus Opecarcinus Kropp and Manning, 1987, like its host coral family Agariciidae, occurs in both Indo-Pacific and Caribbean seas, and is the only cryptochirid genus with a circumtropical distribution. Here, we use mitochondrial and nuclear DNA gene fragments of Opecarcinus specimens sampled from 21 Indo-Pacific localities and one Atlantic (Caribbean) locality. We applied several species delimitation tests to characterise species diversity, inferred a Bayesian molecular-clock time-calibrated phylogeny to estimate divergence times and performed an ancestral area reconstruction. Time to the most recent common ancestor (tMRCA) of Opecarcinus is estimated at 15−6 Mya (middle Miocene—late Miocene). The genus harbours ~ 15 undescribed species as well as several potential species complexes. There are indications of strict host-specificity patterns in certain Opecarcinus species in the Indo-Pacific and Atlantic, however, a robust phylogeny reconstruction of Agariciidae corals—needed to test this further—is currently lacking. The Indo-West Pacific was inferred to be the most probable ancestral area, from where the Opecarcinus lineage colonised the Western Atlantic and subsequently speciated into O. hypostegus. Opecarcinus likely invaded from the Indo-West Pacific across the East Pacific Barrier to the Atlantic, before the full closure of the Isthmus of Panama. The subsequent speciation of O. hypostegus, is possibly associated with newly available niches in the Caribbean, in combination with genetic isolation following the closure of the Panama Isthmus.
Simmonds, Sara E.; Fritts‐Penniman, Allison L.; Cheng, Samantha H.; Mahardika, Gusti Ngurah; Barber, Paul H.(
, Ecology and Evolution)
Abstract
The fluid nature of the ocean, combined with planktonic dispersal of marine larvae, lowers physical barriers to gene flow. However, divergence can still occur despite gene flow if strong selection acts on populations occupying different ecological niches. Here, we examined the population genomics of an ectoparasitic snail,Coralliophila violacea(Kiener 1836), that specializes onPoritescorals in the Indo‐Pacific. Previous genetic analyses revealed two sympatric lineages associated with different coral hosts. In this study, we examined the mechanisms promoting and maintaining the snails’ adaptation to their coral hosts. Genome‐wide single nucleotide polymorphism (SNP) data from type II restriction site‐associated DNA (2b‐RAD) sequencing revealed two differentiated clusters ofC. violaceathat were largely concordant with coral host, consistent with previous genetic results. However, the presence of some admixed genotypes indicates gene flow from one lineage to the other. Combined, these results suggest that differentiation between host‐associated lineages ofC. violaceais occurring in the face of ongoing gene flow, requiring strong selection. Indeed, 2.7% of all SNP loci were outlier loci (73/2,718), indicative of divergence with gene flow, driven by adaptation of eachC. violacealineage to their specific coral hosts.
Adam, Carolina de Lima; Toonen, Robert J.; Carlon, David B.; Zilberberg, Carla; Barbeitos, Marcos Soares(
, Zoologica Scripta)
Abstract
Scleractinian corals are the main modern builders of coral reefs, which are major hot spots of marine biodiversity. Southern Atlantic reef corals are understudied compared to their Caribbean and Indo‐Pacific counterparts and many hypotheses about their population dynamics demand further testing. We employed thousands of single nucleotide polymorphisms (SNPs) recovered via ezRAD to characterize genetic population structuring and species boundaries in the amphi‐Atlantic hard coral genusFavia. Coalescent‐based species delimitation (BFD* – Bayes Factor Delimitation) recoveredF. fragumandF. gravidaas separate species. Although our results agree with depth‐related genetic structuring inF. fragum, they did not support incipient speciation of the ‘tall’ and ‘short’ morphotypes. The preferred scenario also revealed a split between two main lineages ofF. gravida, one from Ascension Island and the other from Brazil. The Brazilian lineage is further divided into a species that occurs throughout the Northeastern coast and another that ranges from the Abrolhos Archipelago to the state of Espírito Santo. BFD* scenarios were corroborated by analyses of SNP matrices with varying levels of missing data and by a speciation‐based delimitation approach (DELINEATE). Our results challenge current notions about Atlantic reef corals because they uncovered surprising genetic diversity inFaviaand rejected the long‐standing hypothesis that Abrolhos Archipelago may have served as a Pleistocenic refuge during the last glaciations.
Knope, Matthew L.; Funk, Vicki A.; Johnson, Melissa A.; Wagner, Warren L.; Datlof, Erin M.; Johnson, Gabriel; Crawford, Daniel J.; Bonifacino, J. Mauricio; Morden, Clifford W.; Lorence, David H.; et al(
, Journal of Systematics and Evolution)
Abstract
The genusBidens(Compositae) comprisesc. 230 species distributed across five continents, with the 41 Polynesian species displaying the greatest ecomorphological variation in the group. However, the genus has had a long and complicated taxonomic history, and its phylogenetic and biogeographic history are poorly understood. To resolve the evolutionary history of the PolynesianBidens, 152 individuals representing 91 species were included in this study, including 39 of the 41 described species from Polynesia. Four chloroplast and two nuclear DNA markers were utilized to estimate phylogenetic relationships, divergence times, and biogeographic history.Bidenswas found to be polyphyletic withinCoreopsis, consistent with previous assessments. The Polynesian radiation was resolved as monophyletic, with the initial dispersal into the Pacific possibly from South America to either the Hawaiian or Marquesas Islands. From the Marquesas,Bidensdispersed to the Society Islands, and ultimately to the Austral Islands. The initial diversification of the crown group in the Pacific is estimated to have occurred ~1.63 mya (0.74–2.72, 95% HPD), making PolynesianBidensamong the youngest and most rapid plant diversification events documented in the Pacific. Our findings suggest that relatively rare long‐distance dispersal and founder‐event speciation, coupled with subsequent loss of dispersal potential and within‐island speciation, can explain the repeated and explosive adaptive radiation ofBidensthroughout the archipelagoes of Polynesia.
Dudoit, ‘Ale‘alani, Iacchei, Matthew, Coleman, Richard R., Gaither, Michelle R., Browne, William E., Bowen, Brian W., and Toonen, Robert J. The little shrimp that could: phylogeography of the circumtropical Stenopus hispidus (Crustacea: Decapoda), reveals divergent Atlantic and Pacific lineages. Retrieved from https://par.nsf.gov/biblio/10079966. PeerJ 6. Web. doi:10.7717/peerj.4409.
Dudoit, ‘Ale‘alani, Iacchei, Matthew, Coleman, Richard R., Gaither, Michelle R., Browne, William E., Bowen, Brian W., & Toonen, Robert J. The little shrimp that could: phylogeography of the circumtropical Stenopus hispidus (Crustacea: Decapoda), reveals divergent Atlantic and Pacific lineages. PeerJ, 6 (). Retrieved from https://par.nsf.gov/biblio/10079966. https://doi.org/10.7717/peerj.4409
Dudoit, ‘Ale‘alani, Iacchei, Matthew, Coleman, Richard R., Gaither, Michelle R., Browne, William E., Bowen, Brian W., and Toonen, Robert J.
"The little shrimp that could: phylogeography of the circumtropical Stenopus hispidus (Crustacea: Decapoda), reveals divergent Atlantic and Pacific lineages". PeerJ 6 (). Country unknown/Code not available. https://doi.org/10.7717/peerj.4409.https://par.nsf.gov/biblio/10079966.
@article{osti_10079966,
place = {Country unknown/Code not available},
title = {The little shrimp that could: phylogeography of the circumtropical Stenopus hispidus (Crustacea: Decapoda), reveals divergent Atlantic and Pacific lineages},
url = {https://par.nsf.gov/biblio/10079966},
DOI = {10.7717/peerj.4409},
abstractNote = {The banded coral shrimp, Stenopus hispidus (Crustacea: Decapoda: Stenopodidea) is a popular marine ornamental species with a circumtropical distribution. The planktonic larval stage lasts ∼120–253 days, indicating considerable dispersal potential, but few studies have investigated genetic connectivity on a global scale in marine invertebrates. To resolve patterns of divergence and phylogeography of S. hispidus , we surveyed 525 bp of mitochondrial cytochrome c oxidase subunit I (COI) from 198 individuals sampled at 10 locations across ∼27,000 km of the species range. Phylogenetic analyses reveal that S. hispidus has a Western Atlantic lineage and a widely distributed Indo-Pacific lineage, separated by sequence divergence of 2.1%. Genetic diversity is much higher in the Western Atlantic ( h = 0.929; π = 0.004) relative to the Indo-Pacific ( h = 0.105; π < 0.001), and coalescent analyses indicate that the Indo-Pacific population expanded more recently (95% HPD (highest posterior density) = 60,000–400,000 yr) than the Western Atlantic population (95% HPD = 300,000–760,000 yr). Divergence of the Western Atlantic and Pacific lineages is estimated at 710,000–1.8 million years ago, which does not readily align with commonly implicated colonization events between the ocean basins. The estimated age of populations contradicts the prevailing dispersal route for tropical marine biodiversity (Indo-Pacific to Atlantic) with the oldest and most diverse population in the Atlantic, and a recent population expansion with a single common haplotype shared throughout the vast Indian and Pacific oceans. In contrast to the circumtropical fishes, this diminutive reef shrimp challenges our understanding of conventional dispersal capabilities of marine species.},
journal = {PeerJ},
volume = {6},
author = {Dudoit, ‘Ale‘alani and Iacchei, Matthew and Coleman, Richard R. and Gaither, Michelle R. and Browne, William E. and Bowen, Brian W. and Toonen, Robert J.},
}
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