Single-Island Endemism despite Repeated Dispersal in Caribbean Micrathena (Araneae: Araneidae): An Updated Phylogeographic Analysis

Lily Shapiro; Greta J. Binford; Ingi Agnarsson

doi:10.3390/d14020128

Single-Island Endemism despite Repeated Dispersal in Caribbean Micrathena (Araneae: Araneidae): An Updated Phylogeographic Analysis

Lily Shapiro^*, Greta J. Binford, Ingi Agnarsson

^*Corresponding author for this work

Faculty of Life and Environmental Sciences

Research output: Contribution to journal › Article › peer-review

3 Citations (Scopus)

Abstract

Island biogeographers have long sought to elucidate the mechanisms behind biodiversity genesis. The Caribbean presents a unique stage on which to analyze the diversification process, due to the geologic diversity among the islands and the rich biotic diversity with high levels of island endemism. The colonization of such islands may reflect geologic heterogeneity through vicariant processes and/ or involve long-distance overwater dispersal. Here, we explore the phylogeography of the Caribbean and proximal mainland spiny orbweavers (Micrathena, Araneae), an American spider lineage that is the most diverse in the tropics and is found throughout the Caribbean. We specifically test whether the vicariant colonization via the contested GAARlandia landbridge (putatively emer-gent 33–35 mya), long-distance dispersal (LDD), or both processes best explain the modern Micrathena distribution. We reconstruct the phylogeny and test biogeographic hypotheses using a ‘target gene approach’ with three molecular markers (CO1, ITS-2, and 16S rRNA). Phylogenetic analyses support the monophyly of the genus but reject the monophyly of Caribbean Micrathena. Biogeographical analyses support five independent colonizations of the region via multiple overwater dispersal events, primarily from North/Central America, although the genus is South American in origin. There is no evidence for dispersal to the Greater Antilles during the timespan of GAARlandia. Our phylogeny implies greater species richness in the Caribbean than previously known, with two putative species of M. forcipata that are each single-island endemics, as well as deep divergences between the Mexican and Floridian M. sagittata. Micrathena is an unusual lineage among arachnids, having colonized the Caribbean multiple times via overwater dispersal after the submergence of GAARlandia. On the other hand, single-island endemism and undiscovered diversity are nearly universal among all but the most dispersal-prone arachnid groups in the Caribbean.

Original language	English
Article number	128
Journal	Diversity
Volume	14
Issue number	2
DOIs	https://doi.org/10.3390/d14020128
Publication status	Published - 10 Feb 2022

Bibliographical note

Funding Information:
5. CoOnculru wsioonrks, combined with previous biogeographic analyses, substantiates Micrathena spiders as an excellent model for Caribbean biogeography of a dispersal-prone lineage. The additional depth in taxon sampling of Micrathena and the related genera, especially across Central and South America, as well as expanded data with next-generation sequencing and the greater availability of fossil evidence for calibration, will add to the res-toluthationMicof ratfhaecntaors in, whiflleuencipotenng biodtially diversispeirtsyalin t-limhiitsedregiduon.e to its size and morphology, have nevertheless been carried across oceanic barriers to colonize Caribbean islands five times i5. Conn 30 mcilusllioinonys ears, perhaps as juveniles. We found interesting evidence for single-island endemWices pinreMse.nfot raci pdaettaaailnedd hmavoeleucunlvaeri lpedhythloegcernyepttiicc adnivde rbsiiotygeinogMra.psahgiict taatnaaalynsdisw oitfh Minicthrae- gtheennuas, adletomgoenthsetrr.atFiunrgt htheratsttuhde igesrowuipll lfiokceulys oconlotanxioznedom thice eCxaarmibibneaatino nresgoifopno mteunlttiiapllsep teimcieess independently during the last 30 million years, and that diversification was likely a result of multiple overwater dispersal events and not GAARlandia vicariance. This finding suggests that Micrathena, while potentially dispersal-limited due to its size and morphology, have nevertheless been carried across oceanic barriers to colonize Caribbean islands five times in 30 million years, perhaps as juveniles. We found interesting evidence for single-island endemics in M. forcipata and have unveiled the cryptic diversity in M. sagittata and Awuitthhoinr Cthoen tgriebnuutiso anlst:oCgeotnhceerp.t uFaulrizthateiro nst,uLd.Si.easn wdiIl.lAf.o;cmuest hoond toalxoognyoLm.Si.ca enxdaIm.Ai.n; asotifotwnsa roef, Lp.oS-. andtential I.A.;specieformals uncoveranalysis, L.S.ed in this phyand I.A.; investigation,logeny. L.S. and I.A.; resources, I.A.; data curation, L.S. and I.A.; writing—original draft preparation, L.S.; writing—review and editing, L.S., I.A. and G.J.B.; visualization, L.S. and I.A.; supervision, I.A. and G.J.B.; project administration, I.A.; funding acquisi- Dispersal probabilities and geography input for BioGeoBEARS, File S2: List of Micrathena species in study, File S3: Comparison of concatenated Bayesian and BEAST phylogenies, File S4: Raw BEAST.xml output file. 1314749 and DEB-1050253 awarded to G. Binford and I. Agnarsson, and by a grant from the National Geographic Society (WW-203R017) to I. Agnarsson.

Funding Information:
This research was funded by the National Science Foundation, grants numbered DEB- 1314749 and DEB-1050253 awarded to G. Binford and I. Agnarsson, and by a grant from the National Geographic Society (WW-203R017) to I. Agnarsson.

Publisher Copyright:
© 2022 by the authors. Licensee MDPI, Basel, Switzerland.

Other keywords

Arachnid
Araneae
Caribbean biogeography
GAARlandia
Long distance dispersal
Micrathena
Phylogeny
Vicari-ance

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10.3390/d14020128

Cite this

@article{baece23682f2431aa6a344c4e0c37250,

title = "Single-Island Endemism despite Repeated Dispersal in Caribbean Micrathena (Araneae: Araneidae): An Updated Phylogeographic Analysis",

abstract = "Island biogeographers have long sought to elucidate the mechanisms behind biodiversity genesis. The Caribbean presents a unique stage on which to analyze the diversification process, due to the geologic diversity among the islands and the rich biotic diversity with high levels of island endemism. The colonization of such islands may reflect geologic heterogeneity through vicariant processes and/ or involve long-distance overwater dispersal. Here, we explore the phylogeography of the Caribbean and proximal mainland spiny orbweavers (Micrathena, Araneae), an American spider lineage that is the most diverse in the tropics and is found throughout the Caribbean. We specifically test whether the vicariant colonization via the contested GAARlandia landbridge (putatively emer-gent 33–35 mya), long-distance dispersal (LDD), or both processes best explain the modern Micrathena distribution. We reconstruct the phylogeny and test biogeographic hypotheses using a {\textquoteleft}target gene approach{\textquoteright} with three molecular markers (CO1, ITS-2, and 16S rRNA). Phylogenetic analyses support the monophyly of the genus but reject the monophyly of Caribbean Micrathena. Biogeographical analyses support five independent colonizations of the region via multiple overwater dispersal events, primarily from North/Central America, although the genus is South American in origin. There is no evidence for dispersal to the Greater Antilles during the timespan of GAARlandia. Our phylogeny implies greater species richness in the Caribbean than previously known, with two putative species of M. forcipata that are each single-island endemics, as well as deep divergences between the Mexican and Floridian M. sagittata. Micrathena is an unusual lineage among arachnids, having colonized the Caribbean multiple times via overwater dispersal after the submergence of GAARlandia. On the other hand, single-island endemism and undiscovered diversity are nearly universal among all but the most dispersal-prone arachnid groups in the Caribbean.",

keywords = "Arachnid, Araneae, Caribbean biogeography, GAARlandia, Long distance dispersal, Micrathena, Phylogeny, Vicari-ance",

author = "Lily Shapiro and Binford, {Greta J.} and Ingi Agnarsson",

note = "Funding Information: 5. CoOnculru wsioonrks, combined with previous biogeographic analyses, substantiates Micrathena spiders as an excellent model for Caribbean biogeography of a dispersal-prone lineage. The additional depth in taxon sampling of Micrathena and the related genera, especially across Central and South America, as well as expanded data with next-generation sequencing and the greater availability of fossil evidence for calibration, will add to the res-toluthationMicof ratfhaecntaors in, whiflleuencipotenng biodtially diversispeirtsyalin t-limhiitsedregiduon.e to its size and morphology, have nevertheless been carried across oceanic barriers to colonize Caribbean islands five times i5. Conn 30 mcilusllioinonys ears, perhaps as juveniles. We found interesting evidence for single-island endemWices pinreMse.nfot raci pdaettaaailnedd hmavoeleucunlvaeri lpedhythloegcernyepttiicc adnivde rbsiiotygeinogMra.psahgiict taatnaaalynsdisw oitfh Minicthrae- gtheennuas, adletomgoenthsetrr.atFiunrgt htheratsttuhde igesrowuipll lfiokceulys oconlotanxioznedom thice eCxaarmibibneaatino nresgoifopno mteunlttiiapllsep teimcieess independently during the last 30 million years, and that diversification was likely a result of multiple overwater dispersal events and not GAARlandia vicariance. This finding suggests that Micrathena, while potentially dispersal-limited due to its size and morphology, have nevertheless been carried across oceanic barriers to colonize Caribbean islands five times in 30 million years, perhaps as juveniles. We found interesting evidence for single-island endemics in M. forcipata and have unveiled the cryptic diversity in M. sagittata and Awuitthhoinr Cthoen tgriebnuutiso anlst:oCgeotnhceerp.t uFaulrizthateiro nst,uLd.Si.easn wdiIl.lAf.o;cmuest hoond toalxoognyoLm.Si.ca enxdaIm.Ai.n; asotifotwnsa roef, Lp.oS-. andtential I.A.;specieformals uncoveranalysis, L.S.ed in this phyand I.A.; investigation,logeny. L.S. and I.A.; resources, I.A.; data curation, L.S. and I.A.; writing—original draft preparation, L.S.; writing—review and editing, L.S., I.A. and G.J.B.; visualization, L.S. and I.A.; supervision, I.A. and G.J.B.; project administration, I.A.; funding acquisi- Dispersal probabilities and geography input for BioGeoBEARS, File S2: List of Micrathena species in study, File S3: Comparison of concatenated Bayesian and BEAST phylogenies, File S4: Raw BEAST.xml output file. 1314749 and DEB-1050253 awarded to G. Binford and I. Agnarsson, and by a grant from the National Geographic Society (WW-203R017) to I. Agnarsson. Funding Information: This research was funded by the National Science Foundation, grants numbered DEB- 1314749 and DEB-1050253 awarded to G. Binford and I. Agnarsson, and by a grant from the National Geographic Society (WW-203R017) to I. Agnarsson. Publisher Copyright: {\textcopyright} 2022 by the authors. Licensee MDPI, Basel, Switzerland.",

year = "2022",

month = feb,

day = "10",

doi = "10.3390/d14020128",

language = "English",

volume = "14",

journal = "Diversity",

issn = "1424-2818",

publisher = "MDPI Multidisciplinary Digital Publishing Institute",

number = "2",

}

TY - JOUR

T1 - Single-Island Endemism despite Repeated Dispersal in Caribbean Micrathena (Araneae: Araneidae)

T2 - An Updated Phylogeographic Analysis

AU - Shapiro, Lily

AU - Binford, Greta J.

AU - Agnarsson, Ingi

N1 - Funding Information: 5. CoOnculru wsioonrks, combined with previous biogeographic analyses, substantiates Micrathena spiders as an excellent model for Caribbean biogeography of a dispersal-prone lineage. The additional depth in taxon sampling of Micrathena and the related genera, especially across Central and South America, as well as expanded data with next-generation sequencing and the greater availability of fossil evidence for calibration, will add to the res-toluthationMicof ratfhaecntaors in, whiflleuencipotenng biodtially diversispeirtsyalin t-limhiitsedregiduon.e to its size and morphology, have nevertheless been carried across oceanic barriers to colonize Caribbean islands five times i5. Conn 30 mcilusllioinonys ears, perhaps as juveniles. We found interesting evidence for single-island endemWices pinreMse.nfot raci pdaettaaailnedd hmavoeleucunlvaeri lpedhythloegcernyepttiicc adnivde rbsiiotygeinogMra.psahgiict taatnaaalynsdisw oitfh Minicthrae- gtheennuas, adletomgoenthsetrr.atFiunrgt htheratsttuhde igesrowuipll lfiokceulys oconlotanxioznedom thice eCxaarmibibneaatino nresgoifopno mteunlttiiapllsep teimcieess independently during the last 30 million years, and that diversification was likely a result of multiple overwater dispersal events and not GAARlandia vicariance. This finding suggests that Micrathena, while potentially dispersal-limited due to its size and morphology, have nevertheless been carried across oceanic barriers to colonize Caribbean islands five times in 30 million years, perhaps as juveniles. We found interesting evidence for single-island endemics in M. forcipata and have unveiled the cryptic diversity in M. sagittata and Awuitthhoinr Cthoen tgriebnuutiso anlst:oCgeotnhceerp.t uFaulrizthateiro nst,uLd.Si.easn wdiIl.lAf.o;cmuest hoond toalxoognyoLm.Si.ca enxdaIm.Ai.n; asotifotwnsa roef, Lp.oS-. andtential I.A.;specieformals uncoveranalysis, L.S.ed in this phyand I.A.; investigation,logeny. L.S. and I.A.; resources, I.A.; data curation, L.S. and I.A.; writing—original draft preparation, L.S.; writing—review and editing, L.S., I.A. and G.J.B.; visualization, L.S. and I.A.; supervision, I.A. and G.J.B.; project administration, I.A.; funding acquisi- Dispersal probabilities and geography input for BioGeoBEARS, File S2: List of Micrathena species in study, File S3: Comparison of concatenated Bayesian and BEAST phylogenies, File S4: Raw BEAST.xml output file. 1314749 and DEB-1050253 awarded to G. Binford and I. Agnarsson, and by a grant from the National Geographic Society (WW-203R017) to I. Agnarsson. Funding Information: This research was funded by the National Science Foundation, grants numbered DEB- 1314749 and DEB-1050253 awarded to G. Binford and I. Agnarsson, and by a grant from the National Geographic Society (WW-203R017) to I. Agnarsson. Publisher Copyright: © 2022 by the authors. Licensee MDPI, Basel, Switzerland.

PY - 2022/2/10

Y1 - 2022/2/10

N2 - Island biogeographers have long sought to elucidate the mechanisms behind biodiversity genesis. The Caribbean presents a unique stage on which to analyze the diversification process, due to the geologic diversity among the islands and the rich biotic diversity with high levels of island endemism. The colonization of such islands may reflect geologic heterogeneity through vicariant processes and/ or involve long-distance overwater dispersal. Here, we explore the phylogeography of the Caribbean and proximal mainland spiny orbweavers (Micrathena, Araneae), an American spider lineage that is the most diverse in the tropics and is found throughout the Caribbean. We specifically test whether the vicariant colonization via the contested GAARlandia landbridge (putatively emer-gent 33–35 mya), long-distance dispersal (LDD), or both processes best explain the modern Micrathena distribution. We reconstruct the phylogeny and test biogeographic hypotheses using a ‘target gene approach’ with three molecular markers (CO1, ITS-2, and 16S rRNA). Phylogenetic analyses support the monophyly of the genus but reject the monophyly of Caribbean Micrathena. Biogeographical analyses support five independent colonizations of the region via multiple overwater dispersal events, primarily from North/Central America, although the genus is South American in origin. There is no evidence for dispersal to the Greater Antilles during the timespan of GAARlandia. Our phylogeny implies greater species richness in the Caribbean than previously known, with two putative species of M. forcipata that are each single-island endemics, as well as deep divergences between the Mexican and Floridian M. sagittata. Micrathena is an unusual lineage among arachnids, having colonized the Caribbean multiple times via overwater dispersal after the submergence of GAARlandia. On the other hand, single-island endemism and undiscovered diversity are nearly universal among all but the most dispersal-prone arachnid groups in the Caribbean.

AB - Island biogeographers have long sought to elucidate the mechanisms behind biodiversity genesis. The Caribbean presents a unique stage on which to analyze the diversification process, due to the geologic diversity among the islands and the rich biotic diversity with high levels of island endemism. The colonization of such islands may reflect geologic heterogeneity through vicariant processes and/ or involve long-distance overwater dispersal. Here, we explore the phylogeography of the Caribbean and proximal mainland spiny orbweavers (Micrathena, Araneae), an American spider lineage that is the most diverse in the tropics and is found throughout the Caribbean. We specifically test whether the vicariant colonization via the contested GAARlandia landbridge (putatively emer-gent 33–35 mya), long-distance dispersal (LDD), or both processes best explain the modern Micrathena distribution. We reconstruct the phylogeny and test biogeographic hypotheses using a ‘target gene approach’ with three molecular markers (CO1, ITS-2, and 16S rRNA). Phylogenetic analyses support the monophyly of the genus but reject the monophyly of Caribbean Micrathena. Biogeographical analyses support five independent colonizations of the region via multiple overwater dispersal events, primarily from North/Central America, although the genus is South American in origin. There is no evidence for dispersal to the Greater Antilles during the timespan of GAARlandia. Our phylogeny implies greater species richness in the Caribbean than previously known, with two putative species of M. forcipata that are each single-island endemics, as well as deep divergences between the Mexican and Floridian M. sagittata. Micrathena is an unusual lineage among arachnids, having colonized the Caribbean multiple times via overwater dispersal after the submergence of GAARlandia. On the other hand, single-island endemism and undiscovered diversity are nearly universal among all but the most dispersal-prone arachnid groups in the Caribbean.

KW - Arachnid

KW - Araneae

KW - Caribbean biogeography

KW - GAARlandia

KW - Long distance dispersal

KW - Micrathena

KW - Phylogeny

KW - Vicari-ance

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U2 - 10.3390/d14020128

DO - 10.3390/d14020128

M3 - Article

AN - SCOPUS:85124733485

SN - 1424-2818

VL - 14

JO - Diversity

JF - Diversity

IS - 2

M1 - 128

ER -

Single-Island Endemism despite Repeated Dispersal in Caribbean Micrathena (Araneae: Araneidae): An Updated Phylogeographic Analysis

Abstract

Bibliographical note

Other keywords

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