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Island biogeography and ecological modeling of the amblypygid Phrynus marginemaculatus in the Florida Keys archipelago



Aim The biogeography of terrestrial organisms across the Florida Keys archipelago is poorly understood. We used population genetics and spatioecological modeling of the Amblypygi Phrynus marginemaculatus to understand the genetic structure and metapopulation dynamics of Keys populations that are otherwise isolated by human development and ocean. Location The Florida Keys archipelago and mainland Florida. Methods We sequenced a 1,238 bp fragment of mtDNA for 103 individuals of P. marginemaculatus from 13 sites in the Florida Keys and South Florida, binned into four regions. We used population genetic analyses to understand the population structure of the species throughout its US range. Furthermore, we used ecological modeling with climate, habitat, and human development data to develop habitat suitability estimates for the species. Results We found clear genetic structure between localities. The Lower Keys, in particular, support populations separate from those in other regions studied. Ecological modeling and genetic analyses showed the highest habitat suitability and genetic isolation in the Lower Keys, but urban development across the species range has resulted in the loss of most historical habitat. Main conclusions A mainland‐metapopulation model best fits P. marginemaculatus gene flow patterns in the Florida Keys and mainland. Ocean currents likely play a role in metapopulation dynamics and gene flow for terrestrial Keys species like P. marginemaculatus, and genetic patterns also matched patterns consistent with geologic history. Suitable habitat, however, is limited and under threat of human destruction. The few remaining pockets of the most suitable habitat tend to occur in parks and protected areas. We argue that conservation efforts for this species and others in the terrestrial Florida Keys would benefit from a deeper understanding of the population genetic structure and ecology of the archipelago.
Ecology and Evolution . 201 8 ;1–1 3 . 
Revised:14Ju ne2018 
DOI:10.1002/ece 3.4333
Island biogeography and ecological modeling of the amblypygid
Phrynus marginemaculatus in the Florida Keys archipelago
Kenneth J. Chapin1| Daniel E. Winkler2| Patrick Wiencek3| Ingi Agnarsson3
Thisisanop enaccessarticleundert hetermsoft heCreat iveCommonsAttr ibutio nLicense ,whichpe rmitsu se,dist ributi onandrep roduc tioninanym edium,
provide dtheorig inalworkisproper lycited.
©2018TheAut hors.Ecology and Evolutionpu blishedbyJohnWiley&SonsLtd .
1Depar tmentofEcology&Evolutiona ry
Biolog y,Universi tyofCalifornia,Los
Angeles,LosAngeles,C alifornia
2Depar tmentofEcology&Evolutiona ry
Biolog y,Universi tyofCalifornia,Irvi ne,
3Depar tmentofBiology,Universit yof
Vermont,Burling ton,Verm ont
KennethJ.Chapin,Depar tmentofEco logy
&EvolutionaryBiology,Universit yof
Califo rnia,LosAngeles,LosAngeles,C A.
Funding information
TheodoreRooseveltMemorialFundoft he
AmericanMuse umofNatur alHistory;Edwin
W.PauleyFell owship,UCLA;Department
ofEcolog y&EvolutionaryBiology,UCL A;
Depar tmentofEco logy&Evol utionary
Biolog y,UCI;NationalGeo graphi cSociet y
poorly understood.Weusedpopulationgenetics andspatioecological modeling of
the Ambly pygi Phrynus marginemaculatusto un derstand t he genetic stru cture and
Methods: We sequenced a 1,238bp fragment of mtDNA for 103 individuals of
P. marginemaculatusfrom13sitesintheFloridaKeysandSouthFlorida,binnedinto
four regions. We used population genetic analy ses to understan d the population
structureofthespecies throughout its US range.Furthermore,weusedecological
Results: We found clear genet ic structure b etween local ities. The Lower Keys, in
particular, support populations separate from those in other regions studied.
Main conclusions:A mainland-metapopulation model best fits P. marginemaculatus
inmetapopulationdynamicsandgeneflowforterrestrialKeysspecieslikeP. margin-
fewremainingpockets ofthemostsuitable habitattendtooccurinparksandpro-
tected areas.Weargue that conser vation efforts for this speciesandothers inthe
Present address
Depar tmentofEcologyandEvolutionary
Biolog y,Tucson,Arizona.
   CHAPIN et Al.
the evolut ionary his tory of life (Ma cArth ur & Wilson, 1967; Podas,
This is par ticularly su rprising conside ring the Florid a Keys was the
ory (e.g., Mac Arthur&Wilson, 1967;Simberloff, 1976;Simberloff &
Wilson,1969,Simberloff&Wilson1970;Wilson&Simberlof f,1969).
The Florida Keys may support metapopulation spatial struc ture
for some species or genetic divergence and speciation in others
(Hanski, 1998; S hrestha, W irshing, & Har asewych, 2015 ). In either
case,thedistributionofspeciesacrosstheKeysisimport antforun-
derstanding both specieslong-termsur vivaland biodiversity.Thisis
especiallytrue considering the precariousness ofFlorida Keys habi-
tat sinthef aceofhumandisturbance,includinghumandevelopment,
deforestation,nonnativespeciesintroductions, andhuman-induced
climate change impacts like sea level rise, increased catastrophic
storms, and altered fire regimes (Bancroft, Strong, & Carrington,
LoboSternberg,1994;Ross, O’Brien,Ford,Zhang, &Morkill,20 09).
Fur the rm or e, th eFlo ri daKey sr em ai namaj or to ur is td es tina ti on wi th
Our understanding of the genetic structure of Florida Keys or-
current s play a major role in gene flow and migration (Apodaca,
patter ns of terrest rial specie s are expec ted to differ co nsiderabl y,
as the mari ne ecosystem a cts as an uninh abitable mat rix and the
formation of terrestrial habitat occurred on different timescales
Geneti c research using n ative terrest rial species i s scarce, but
not absent . The mosqu ito Aedes aegyptishowednogeneticstruc-
ture along the Florida Keys,likely because they disperse via flight
(Brown, O bas, Morley, & Powell , 2013). The invasive br own anole
(Anolis sagrei) and greenhouse frog (Eleutherodactylus planirostris)
showed introductions to the Florida Keys from Cuba but cannot
inform patterns for nativespeciesacross the Keys (Heinicke, Diaz,
& Hedges, 2 011; Kolbe etal. , 2004). An alloz yme elect rophoretic
study ontheFloridaTreeSnail (Liguus fasciatus)revealedlowlevels
ofgenetic diversity, likely duetoa recent introductionfrom Cuba,
1991).ThelandsnailCerion incanumshowedsomehaplotypestruc-
that the C. incanumspread southwesterly to colonizenew Keys as
anyinvestigatedhumanimpact sonstructureandconnectivity.
The human population of the Florida Keys has drastically im-
pacted ecosystems therein. The human population of Monroe
County, which includes the Florida Keys and a portion ofrural land
(US Census B ureau). While po pulation sizes of re sidents may have
stabilized over the last 25years (currently ca. 77,000 residents),
the numb er of tourists vis iting the Keys is enor mous. In 2014, an
estimated 4.516million tourists visited the Florida Keys (Key West
Ch am berofCo mm erc e, 20 17 ). KeyWe st, thema jo rc ity of th eF lor id a
Keys,locatedonanisland ofonly 19km2,hasover52,000housing
units. T he natural are as that remain are m ostly protec ted as state
parks or n ational wildlife r efuges, but are co ntinually impa cted by
nearb yhuma nact ivit y(P eterson,L opez,Frank,P or te r,&Silvy,20 04).
Weused fieldobservationscoupledwithlanduseandclimate
data to model Phrynus marginemaculatus distribution in South
Florida a nd the Florida Keys . Species dis tribution mo dels (SDM)
have been employed in many conservation, evolutionary, and
ecologic al applications (Elith & Leathwick, 20 09). These include
studiesofspatial patternsof diversity(Hoagstrom,Ung,&Taylor,
2014;Peterson, 2011;Walt ari&Guralnick,2009) ,genetic struc-
ture (Gotelli & Stanton-Geddes,2015),and the historicspread of
Meentemeyer,2012). Additionally, SDM have identified suitable
climaticfactorsdrivingspeciesdistributions, including responses
toclimatechange(Feng&Pap eş,2015;Ficeto la,T huiller,&Miaud,
2007). Ad ditionally, SDM tech niques have advanc ed in the past
decade (Guisan & Thuiller, 2005) to allow for predictive power
with presence-only data (Bradley, 2015; Bradie & Leung, 2016;
Elithetal.,2006; Jiménez-Valverde,Decae, &Arnedo, 2011)and
P. marginemaculatuspopulationsintheUS.In particular,weaimed to
uncover the genetic structureofthe speciesacross theFlorida Keys
inrelationtothe speciesrangevia phylogeneticanalysis,and identify
species’ potentialrange.Together,theseresultswillbe thefirst toex-
amineP. marginemaculatusinthewild,andwillprovidecritic alinforma-
ti o napp l i c abl e tom a nyt e r res t r i ali s lan d s peci e san d t hei r con s e r v ati o n .
2.1 | Study site
The FloridaKeysisaca250-km-longarchipelagoamountingtoca
CHAPIN e t Al.
Florida s outhwest to Key West 140km f rom Cuba. The Keys ar e
made from t wo geologic form ations that both for med during the
Tarantian Pleistocene (0.126–0.0117mya) and raising above sea
level during the Wisconsin glaciation (ca. 100,000 before present;
(Bahia HondaKey to Key Largo), however,are constituted of fossil
coralreefs(termed KeyLargoLimestone)withoutstrong lateraliza-
Florida m ixed hardwoo d forests h ave persiste d since the bir th
orwestfromtheC aribbeanandBahamas,asFloridawasnevercon-
nected totheCaribbeanislands (Snyder,1990).Thus,we might ex-
dispers e over water, and temper ate species o nly able to est ablish
allofwhichhave Caribbeanorigins. That being said,natural migra-
introduced via humans, and still others have gone extinct(atleast
locall y) since their discover y (Snyder, 1990). Inver tebrate biogeo-
graphicpatternsare more mixed, but still fit themodel of tropical
Florida ant species have Nor th American origins,while Butterflies
Land to support the growing humanpopulations of Miami and
acentury (Small, 1929).The firstsettlers in Southern Floridawere
concentrated in the Florida Keys. Early settlers exploited pineand
hardwoo d trees (espe cially Mahog any) for lumber, fue l, and slash-
and-burn agriculturalpractices(Small, 1917;Browder,Littlejohn,&
Young,1976;Wilson&Porras, 1983).Asa result,very few stands
of rocklan d include origi nal forest. In dustrial log ging was enabl ed
by the Flor ida East Coa st Railroa d, which reac hed Miami in 1896.
Rocklan d habitat was subje ct to clear-cutting fo r timber and fuel
but made pooragricultural land due to an abundance of limestone
agricultural access. Lime stone rocks co llected via h and, plow, and
mine, were used as buildingmaterials andcanbeseeninhistorical
building s, walls, an d gardens of th e Florida Keys to day.Ro cklands
ecosystem, and are often dominated byinvasive species (Loope &
Dunevit z,1981).Theabilityto turn rocklandintospaceforagricul-
ture and housing has led to the steep decline in rockland habit ats
that conti nue to the pres ent, with p ractic ally no hope of r eestab-
lishment without human inter vention (Dorn,1956;Meyers& Ewel,
2.2 | Study species
We used the amblypygid species P. marginemaculatusC.L.Koch,
1840 as amodel to understandthegeneral biogeographicpattern
ofterrest rialFloridaKeysspecies.Amblypygidsareasmallar achnid
order(ca.220spp.)oflarge nocturnalpredators(Chapin&Hebets,
2016).Phrynus marginemaculatusistheonlyamblypygidspeciesin
speciesofamblypygid(Chapin&Hebets,2016;Figure1).Laborator y
research has shown that P. marginemaculatus exhibit ritualized
agonisti c displays (Fowle r-Finn& H ebets, 2 006), and ca n learn to
navigatemazesusingtactilecues(Santer&Hebets,2009a, 2009b)
via exceptional brain structures and sensory systems (Chapin &
Hebets,2016;Santer&Hebets,2011).Whilef ascinatinglaboratory
researchhasbeen conduc ted on the species, no researchontheir
habitat requirements, distribution, population ecology, or popu-
lation gen etics has ever be en published (C hapin & Hebet s, 2016;
Weygoldt,20 00).
Historical records indicate that the species was found as far
cies is also foundon severalBahamian islands, Cuba,Jamaica,and
Hispaniola(Muma,1967;Quintero,1981).Research onthespecies,
FIGURE1 PhotographsoftheamblypygidPhrynus
highlight scolorationandpat terning
5 cm
   CHAPIN et Al.
&Hebets, 2006;Spence &Hebets20 06; Santer & Hebet s,2009a,
Interestingly, P. marginemaculatus has evolved a plastron to
& Chapman , 2000 ). While the fu nction of th e plastron i s not well
unders tood, it likely i ncreases chan ces of surviv al during floo ding
in their terrestrial retreats. This may be particularly impor tant in
the Flor ida Keys, where annua l hurricanes c an result in floodi ng.
Furthermore, hurricanes, alongwith ocean currents, likely promote
plastronallowingunderwaterbreathinglikelyextends thedispersal
propens ities across b odies of water, and th e likelihood of su rvival
duringoceanmigration,inP. marginemaculatus.
Twomolecular phylogenetic studies have focused on amblypy-
gids. First, a phylogeny of the Damon variergatusgroup delineated
two crypticspecieswithinDamon,an African genus of amblypygid
diversit yacross cavepopulations(Espositoetal.,2015).In par ticu-
lar,Espositoetal.(2015)notedhigh levels ofdiversityacrossmito-
sequencesto examineifsimilargenetic structure acrosssmallgeo-
2.3 | Specimen collection
Wecollected P. marginemaculatusspecimensfrom13locationsin
anonrandomsamplingmethod( Table1;Figure2).Welimitedour
survey to upland habitat types, as we assumed that P. margin-
emaculatuswouldnotbefoundininter tidalhabitat slikemangrove
swamps an d floodplains. Additional survey areas were selected
habitat types(Table1).P. marginemaculatushideunderdebris,es-
peciallylimestone rocks, during theday (Chapin&Hebets,2016;
trails an d looking for P. marginemaculatusunderrocks,logs,and
other larger debris. When found, we collected genetic samples
andstored them in 95%ethanol ondry ice. Wedissectedmuscle
2.4 | Extraction, amplification, and sequencing
(−20°C) anda50-mLfinalelution. Weamplified a1, 238nucleotide
sequenceofthemitochondrialgenecy tochromecoxidasesubunit1
initialcycleof 2minat 94°Cand ending with10minat72°C.Using
illustraPuReTaqReady-To-GoPCRbeadsand40 0-nMforwardand
reverse primers,the longor shor t read of COI was sequenced for
eachsample.LCOI1490wasuse dast heforwardprimerforbotht he
fortheshort readsandC1-N-2776wasusedasthereverse primer
fo r t he lo ngre a ds (LCO I14 90 GG TCA AC A A ATC ATA A AG ATAT TG G ,
GGATAATCAGAATATCGTCGAGG; Folmer, Black, Hoeh, Lutz, &
more informative than nuclear DNA among Amblypygi (Esposito
2.5 | Cleanup and alignment
Core and Genewizfor sequencing. Subsequently sequences were
assembled using the Chromaseq module (Maddison & Maddison,
2016a) in Mesqu ite 3.02 (Maddiso n & Maddison, 2016b) th rough
Phred and P hrap (Ewing & Green , 1998; Ewing, Hilli er, Wendl, &
Green,1998; Green,1999;Green&Ewing,2002), and thenproof-
read in Me squite. Seq uences were a ligned with C lustal W2 (Larkin
2.6 | Genetic analysis
Wegroupedlocalitiesintofourregionsbymajorgeologic features:
the mainland, Key Largo, Upper Keys (excluding Key Largo), and
LowerKeys.Weproducedgeneticdiversit yindicesforeachregion
and used a hierarchical analysis of molecular variance (AMOVA;
pop N H G λ λc Hexp π
LeyLargo 18 2.44 8.53 0.883 0.935 0.032 0.003
Mainland 28 3.12 20.63 0.952 0.987 0 .105 0.010
UpperKeys 13 2.56 13.0 0 0.923 1.000 0.150 0.013
LowerKeys 44 3.54 28.47 0.965 0.987 0.115 0.010
Tot al 103 4.39 6 7. 57 0 .985 0.995 0.131 0.013
Note. GisSto dda rtan dTa yl or ’s in de xo fM LGd ivers it y;His th eS ha nno n–W ie ne rI nd exof mu lt il ocus
genotype(MLG)diversity;Hexpis Nei’sunbiased genediversity; πisnucleotidediversity; Nist he
TABLE1 Geneticdiversityindicesof
Phrynus marginemaculatus occur
CHAPIN e t Al.
and betweenlocalities and regions. Wetested for isolation by dis-
tance (IBD) by testing for a correlationbetween Nei’s genetic dis-
tance and maximum geographic distance among samples with a
mantel tes t (Mantel, 1967). We used disc riminant ana lysis of prin-
cipal components (DAPC)with cross-validation to examinegenetic
divergencebetweenregionsandcalculatedpairwise GSTasanes-
timate ofmigrationbetween regions. WeusedtheR2.3.2 (R Core
2008; Jombar t & Ahmed, 2011), “mmod” (W inter, 2012), “pegas”
(Paradi s, 2010), and “poppr” ( Kamvar, Brooks, & Gr ünwald, 2015;
2.7 | Ecological modeling
timatethegeographicrangeofP. marginemaculatususingtheniche
modeling software Maxent 3.3.3 (Phillips, Anderson, & Schapire,
2006;Phillips &Dudík,2008).Maxent usesamaximum-entropyal-
gorithm to predict species geographic ranges using presence-onl y
erswereobtainedfromtheUnitedStatesGeologicalSurvey(http:// We ran a second set of models thatincludedland
usedatabased onimagerymadepublicallyavailable bytheFlorida
DepartmentofEnvironmentalProtection(http://geodata.dep.state. This dataset included 195categories ofland use based pri-
tation corridors) but alsoincluded subcategoriesofvegetation and
other ecologically relevanthabitattypes (e.g., pinelands, mangrove
swamps, cabbage palm hammock). This included all land cover
categories used in the Florida L and Cover Classification Systems
All data we re clipped to a regi onal extent of so uthern Flori da
and the Fl orida Keys at app roximately la titude 28° N using ArcG IS
v10.2.2 . This nor thern latit ude is locate d approximate ly along the
indicatethatP. marginemaculatusoccurs beyond thisline(Quintero,
area using t he package ‘Raster’ in R 3.3 .2 (Hijmans & van Ette n,
coefficients under |0.75|. Theseclimate variables represent annual
itation.Temperaturevariables included annual mean temperature,
mean diurnalrange, isothermality,and mean temperaturesofboth
the wettest and driest quar ters. Precipitation variables included
annual temperature, precipitation during the wettest and driest
months, precipitationseasonality,andprecipitation ofthewarmest
We ran 100 model replic ates using a randoml y selected 75%
of the occur rence record s to calibrate t he model an d 25% to test
it(Phillips etal., 2006),wellbeyond the ideal minimumsample size
toobt ainreliable results(Proosdijetal.,2016).Each model was as-
sessed with the area under the receiver operating characteristic
curve (AUC;Hanley &McNeil,1982).AUCvaluesrepresent amea-
sure of the MaxEnt model’s ability to discriminate betwe en suit-
able and unsuitable areas in the modeled distribution (Anderson
& Gonzal ez, 2011). AUC values ra nge from zero to one, w ith one
indicating a perfect differentiation of suitable and unsuitable hab-
itat.Wecompared predicted models against distribution literature
for P. marginemaculatus (Quintero, 1981). Models that performed
poorly (AUCscores<0.75)orthatvaried substantiallyfromhistor-
ical recordswere discarded. Jackknife tests were usedtoevaluate
FIGURE2 MapofSouthernFlorida
linesindicatelowerGSTt;Gst range:
   CHAPIN et Al.
the impo rtance of eac h environment al and abiotic var iable to ex-
plain the range ofP. marginemaculatus.Last,we calculated areas of
overlap between human land use features (i.e., urban and rural
developments, transportation, communication, and utilities, and
agricultural lands) and model outputs of suitable habitat using the
image-processing software ImageJ (Abr amoff,Magalhaes ,& Ram,
2004).Wecalculated declinesin suitablehabitat atfourthresholds
ofmodeledsuitablehabitat (>0.1, 0.1, 0.3,0.5, and 0.9)caused by
3.1 | Population genetics
Wesequenceda1, 238bp region ofthemitochondrialCOIgeneof
netic dive rsity ( Table1).A dditional ly,a r ange-wide mante l test for
(Mantelr =−0.07,P = 0.637).AhierarchicalAMOVArevealedpopu-
lation st ructure a mong popula tions, but not r egions (Table2). The
AMOVAindicated significant genetic structure between localities,
suggesting that oceans limit dispersal. Stratified cross-validation
of DAPC resul ted in a mean success ful assignment of 0.92% a nd
structure (Figure3). Furthermore, pairwise GST showed relatively
high divergence of KeyLargo localitiesfrom the rest ofthe range,
and low divergence between mainland and island sites, indicating
3.2 | Ecological modeling
Specie s distribut ion modelin g using MaxEnt fou nd good mode l fit
for climate-only models (mean AUC=0.978±0.02, n = 100 m od-
els;Figure4a–c).Habitatsuitabilitywas highestin the FloridaKeys
(Figure4), bu t also exten ded to the so utheaste rn end of mainl and
Florida. Areas of predicted suitable habitat on the southeastern
mainland corresponded to the geologic features of the peninsula,
which had a p ermutation importance of 5.8%. H owever, suitabl e
habitat was identified primarily by environmental variables that
contribu ted most to the mo del: precipit ation of the colde st quar-
ter(74.8%permutationimportance)andmeandiurnal temperature
range (14.7%). Altit ude also had predi ctive power with 2 .4% per-
mutatio n import ance in the fir st set of models . Jackknife te sts of
Models including land use categoriesperformed slightly worse
(mean AUC=0.873±0.06, n=100 models) than those without
landusebutappeartohaverefinedthehabitatsuitabilityofP. mar-
ginemaculatus (Figure4d–f). L and use categories had the highest
the drie st quarte r (18%),m ean diurnal t emperatu re range (12.7%),
TABLE2 Hierarchicalanalysisofmolecularvariance(AMOVA)
σ% variance ϕp
Withinlocalities 1.377 38.37 0.616 <0.001
Betweenlocalities 1.9 97 55.65 0.592 <0.001
Betweenregions 0. 214 5.97 0.060 0 .160
FIGURE3 Discriminantanalysisof
DA eigenvaluesPCA eigenvalues
CHAPIN e t Al.
geology(7%),andaltitude (3%). Similarto our modelswithout land
use catego ries, annu al mean tempe rature had t he highest t raining
temperature during the driest quarter, mean diurnal temperature
range, an d mean temper ature of the war mest quar ter followed in
ter msofvaria bleim port anceinisolatio n.Mod elswithlanduseiden-
tified regions of the Lower andUpper Keys, pockets in Everglades
National Park,andseveral coastal areas ofMiami asthe most suit-
ablehabitat.Additionalsuitableareas wereidentifiedon KeyLargo
and in Big CypressNational Preserve.Smaller pockets ofpotential
habitatrangeduptheeastandwestcoast s.
We saw an alarm ing 22%–34% human-ind uced declin e in suit-
able habitat under the best fit model (Figure5; Tables3 and 4).
indicates that, while climatically identified habitat shows consid-
erable decline, humanimpac ts particularly target landuse habitat
FIGURE4 MaxEntsuitabilitymapforP. marginemaculatusinsouthernFlorida.Colorscaleindicatesprobabilityofoccurrencebasedon
   CHAPIN et Al.
Pine rocklands succeedtotropicalhardwoodhammocksafter two
or three decades of fire suppression (Loope & Dunevitz, 1981;
Robertson, 1981), but it remains unclearif P. marginemaculatus oc-
naturally in rockland habitats (Snyder etal., 1990) and P. margin-
(Hofstet ter,1975;Robertson,1953,1962),have evolvedto survive
The mainland and Lower Keys show the greatest genetic di-
versity.This is likely because these tworegionsincludethelargest
able habitatwithin an inhospitablematrix. Key Largoshowed rela-
tively low diversity,despite the island’ssize.However,onlya small
portionof Key Largo’slandareaissuitable habitat—mostoftheis-
Genetic variation was significant between localities but not
larger regions (Table2), suggesting a more complicated genetic
st ru cturethanouraprioriregionaldeline at io ns .Pop ul at io n- leve lg e-
neticstruc tureisalignedwithintuition,consideringallpopulationsin
ourstudyoccuronKeysorislandsofhabitatsurrounded byhuman
disturbance (Figure2). Regional structure, however, is somewhat
surprising.Weselectedregionsa prioribasedongeologicfeatures:
theKey Largo regionforitssizeand proximityto themainland;the
Upper an d Lower Keys for the ir geologic va riation in fo rmation, if
island populations.This generally alignswith the population struc-
ture of nati ve Cerionland snails, which showed isolation between
the Uppe r and Lower Keys (Shre stha etal., 2015 ). Species on th e
LowerKeyslikelyhaveauniqueevolutionar yhistoryseparatefrom
withkeypopulationsallbeingclosestrelatedtomainland localities.
This pat tern suggest s that a mainland–met apopulation m odel de-
scribedthelandscapegenetics oftheKeys.Asmentioned,genetic
Keydivision(Shresthaetal.,2015). But researchon marinespecies
like bicolor damselfish (Eupomacentrus partitus) and common reef
sponge(Callyspongia vaginalis)foundmuchlowerlevelsofdivergence
betweenregions than we found for P. marginemaculatus(DeBiasse,
Richards,& Shivji,2010; Lacsonetal.,1989).Thisis likely because
P. marginemaculatus is much more disper sal limited tha n a marine
study.Thismatching patternsupport stheideathatcurrents playa
majorroleinP. marginemaculatusgeneticstructure.
PairwiseGSTshowedthat thegreatest divergencewasbetween
Key Largo an d the other region s (Figure2). This coul d be caused
bymigrants from the Bahamas, the closestislands ofwhichareca.
100km from Key Largo.Surprisingly,the mainlandhad low Gstes-
timates with the Upper and LowerKeys. We posit that this is due
toongoinggeneflow betweentheseregions. Ocean currentslikely
push raftingP. marginemaculatustotheLowerKeysasmightmajor
weather events including hurricanes (Fleming & Murray, 2009).
Experim entswit hGPS-equi pp edbuoyss howthatt hisisamajorcur-
rentpathway(Lee&Smith,2002)andP. marginemaculatus,withthe
threemarineinver tebratesshowedhighgeneflowandconnectivit y
2007).Thesaltmarshsnake(Nerodia clarkii),whichissomewhatre-
FIGURE5 (a)MaxEntsuitabilitymapofthebestfitmodel
amblypygidPhrynus marginemaculatusintheFloridaKeysandSouth
0.00 0.92 100 km
10 km
CHAPIN e t Al.
andLowerKeysthatwasexplainedby IBD (Jansenetal., 2007).In
general,ourSDMpredictedhabitatsuitabilityforP. marginemacula-
ties. This limited range generally matches museum records, with
occasionalrecords fromcountiesasfar NorthasCharlot te county
(Quintero,1981).Thesenor therlyreco rdscouldbef romsparsep op-
be made by va grant alloa nthropic ind ividuals as sociated onl y with
human st ructures , and not viabl e populations . Additional ly,mo del
predic tionso fhab it at su it abilitywith inth eurb an ar ea sofsouth ea st-
blehabitatismuchlessbecauseofhumandevelopment .
Few studies of Florida biogeography have been conducted,
but generally align withourresults.Ant gut microbiota show simi-
largenetic structurebetweentheUpper andLowerKeys,but also
shoe divergenceamongthe Lower Keys, which might be indicative
of Carib bean migration (Hu e tal., 2014). The mosquito A. aegypti
showed practically no genetic stru cture among the Florida Keys,
likelybecausetheydisperse viaflight(Brownetal.,2013).Shrestha
etal. (2015) proposed that the C. incanum spread southwesterly
tocolonize new Keys as theyformed, withLower Key populations
beingtheyo ungest.L astly,antg utmicr obi otashowedgeneticst ruc-
pinerocklandsasthemostsuitablehabitattypesforP. marginemac-
andiscorroboratedbypublished collection sites of the speciesfor
laborat ory resea rch (Hebets & C hapman, 20 00; Weygoldt , 2000).
The two ha bitat types , being at relativel y high elevation, ar e the
primar ytargetsforhuman development inFlorida (Noss,LaRoe,&
Scott , 1995;Snyde r etal., 1990). Thu s, our mode ling result s show
that P. marginemaculatus suitable habitats are also areas where
human disturbance has been, and continues to be, an imminent
Pinerockland forests,oncecommon throughout southeastern
Florida,arenowoneofthe mostthreatenedhabitats globally,with
atleast98%globalloss(Nossetal.,1995).Thisincludesca.8,0 00ha
in Everglades National Park and a mere 920ha outside the park’s
bounda ry (Bradl ey,20 05). Pine roc kland habit at was identif ied as
includedlandusecategoriesbutalsothose with onlyclimatevari-
ables and geolog y.Pine rockland habitats occur on exposed lime-
stonesubstrates where limestone rock outcroppings are common
andprovideimportantmicrohabitatforP. marginemaculatus(Chapin
&Hebets, 2016;Hebets& Chapman,2000).Humandevelopment,
fire supp ression, and climate change have altered or ent irely re-
This habitatlosshasresulted in fivefederallylistedanimal and 21
rare, endemicplantspeciessympatricwithP. marginemaculatus, all
ofwhicharedependent on remaining fragments of pine rockland
habitat (FloridaNaturalAreasInventory,2010).Furthermore,lime-
stonerocksthatmakeupcriticalhabitatforP. longipesareoftencol-
Some are as of pine rockland a nd upland hardwo od forest are
protectedtoday.Theseinclude patcheswithin EvergladesNational
Park, Big Cypress National Preserve, Key Deer National Wildlife
Refuge,andst ate-m an agedlands .M os th abita to ut sid eofthe se pr o-
tectedareashavealreadybeendestroyed,andmanysur vivingfrag-
Florida Keys.Thishasdramaticimplications forP. marginemaculatus
andtheendemic,endangeredcommunit yinwhichtheyoccur.
Human development is not the only threat to pine rockland
and uplan d hardwood for est habitat s; sea level ris e brought on by
human-induced climate c hanges is also threatening these habitats
TABLE3 AreaofsuitablehabitatoftheamblypygidPhrynus marginemaculatusinsouthernFloridaandtheFloridaKeys.Areaofhabitat
habitatatagiventhresholdbyhumandevelopment.ModelfitisindicatedbytheAreaUndertheCur veandst andarddeviation(AUC±SD)
0.1 threshold 0.5 threshold 0.9 threshold
AUC ± SDkm2% loss km2% loss km2% loss
Climateonly 3,545.88 27. 5 8 179.95 3 4.91 4.64 22.44 0.978±0.02
Climate+landuse 2 , 42 7.96 48.68 3 00 .97 43. 81 12 .74 28.65 0.873±0.6 0
TABLE4 Reductioninsuitablehabitatfortheamblypygid
Phrynus marginemaculatuspredictedbyMaxEntmodelingcausedby
Threshold Habitat DevelopmentaPercent loss
0.1 3,545.88 2, 5 67. 7 9 27. 5 8
0.3 532.32 400.15 24.8 3
0.5 17 9.9 5 11 7.1 2 34 .91
0.9 4.64 3.60 22.44
0.1 4, 247.9 6 2, 17 9.85 48.68
0.3 958. 57 558.18 41.7 7
0.5 30 0.97 1 69.11 43.81
0.9 12.74 9.0 9 28.65
   CHAPIN et Al.
(Maschinskietal.,2011;Rossetal., 2009).Inthissense,increases in
thefrequencyandintensit yof hurricane stormsurges reshapepine
rockland and similar vegetatio n communities (Ross etal., 1994). It
remains unknown how climate-induced changes in storm systems
may have alrea dy impacted the co nsiderably fr agile extant P. ma r-
studie s of other species . For example, Hu rricane An drew dramati-
cally al tered pine roc kland commu nities when i t struck po rtions of
Everglade s National Par k and Big Cypres s National Pre serve, lea d-
ingto ca.90%mortalityofmaturepinetrees(Maguire,1995)which
negative ly impacted p lant and animal co mmunities (L loyd & Slater,
2012; Orr & Ogden, 1992; Williams, Wang, Borchetta, & Gaines,
2007). Majorstorms and humandisturbance not only alterhabitats
butcanalsoleadto isolationof populationsandreshape population
geneticsofspeciesatrisk(e.g.,Villanova,Hughes,&Hof fman,2017).
Ourresearchwason specimenscollectedin2015, priortothe 2016
Hu rri can eM att h ew and20 17Hu rr i can eI rma ev ent s.Fu t ur ere se a rc h
willbenefitfromexaminingtheimpactsoftheseandothers tormson
populationstructureofP. marginemaculatusinsouthernFlorida.
Both our genetic and ecologicalresultsare limited byour data-
set, whichis constrained in both time andspace. Spatially, we only
sampledP. marginemaculatusinso uther nFl oridaandtheFloridaKeys
archi pe la go,butt hespeciesoccu rs asfarso ut hwes tasHi sp aniola,in -
clud in gp op ulation si nt he Ba ha mas ,Cub a, Ja maica ,a nd th eTu rksan d
Caicos (Quintero, 1981). In par ticular,gene flow fromthe Bahamas
and Cuba to Key L argo and th e Lower Keys could be o ngoing, but
patterns. While historicalmaterial wouldincreasesample sizes, our
moderncollections spanthespatialrangeof Floridahistorical sam-
ples bar northern limits, where populations may no longer occur.
Sampl ingwa sunev enacr osssi tes,w hi chcouldbiasre su lt s.Lastly,w e
usedonlyonesequence inouranalysis. Wechosea mtDNA marker
because nDNA appears highly conser ved in Amblypygi (Esposito
4.1 | Conservation
Our resul ts point to a prima ry threat to the p opulation hea lth of
P. marginemaculatusinthewild:habitatlossbyhumandevelopment.
Approximately 77,000 people permanently reside in the Florida
Keys (US Censu s Bureau). Given th e small land area of t he archi-
pelago, thisaccountsfor an average density of 205.54peopleper
squarekilometerand leavesapproximately150km2uninhabitedby
humans, muchof which isseasonallyorpermanentlyflooded habi-
tat unsui table for ma ny terrest rial specie s. Furthe rmore, th is does
notinclude the impactfromcommercial,transportation,andutili-
ties developments. Fortunately, muchof the remaining habitat for
P. marginemaculatus is within protect ed areas managed by f ederal
andstateagencies.This,however,doesnotprotecthabit atsfromall
threats,includingtheimpact sofincreasedhurricanes,sea-levelrise,
Secondarily,P. marginemaculatus is collec ted from the wild f or
saleinthepettrade. While we donothavedataon the numberof
individualscollectedforsaleinthepetindustr y,personal obser va-
WildpopulationsofP. marginemaculatuswouldbenefitfromcaptive
breedin g that allows thes e fascinating an imals to be kept as pet s
without reducingnumbersin the wild.Moreresearch on wild pop-
ulations is n eeded to asse ss populati on health, a nd we encoura ge
researchers to conduct both fieldand laboratorystudieson these
Major funding was provided by theTheodoreRoosevelt Memorial
provided b y the Edwin W. Pauley Fello wship, UCLA , Departm ent
ofEcology & EvolutionaryBiology,UCLA ,Department ofEcology
& Evolutiona ry Biolog y,UCI a nd the Nationa l Geograph ic Society
(WW-203R-17) to IA. Thanks also to laboratory collections man-
ager Emily Chen, Sarah Hsu, and other undergraduate assistants
for maintaining samples, dissecting tissue for DNA extraction, and
databasingliteraturesearches.Thisresearchwasconducted under
EvergladesNationalPark Scientific ResearchandCollectingPermit
EVER–2014–SCI–0057,Nation alW ildlife RefugeSystem Rese arch
andMonitoringSpecial Use PermitFFO4RFKD–2015–001,Florida
Park Ser vice Scientific Collecting Permit 08051410, and Miami-
K.J.C .conceived thestudy; K.J.C and D.E.W collected and extracted
sa mp le s;I.A. an dP.W.se qu en ce d,clean ed ,a ndalignedDN A; K.J .C .a n-
aly zedgenet icdat a;D.E.W.analy zedecologicaldata;K. J.C.a ndD.E .W.
DNA sequences have been under accession number
MH478912- MH479012.
Kenneth J. Chapin
Abramoff,M. D.,Mag alhaes,P.J.,&R am,S.J.(2004). Imageprocessing
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How to cite this article:ChapinKJ,WinklerDE,WiencekP,
theamblypygidPhrynus marginemaculatusintheFloridaKeys
archipelago.Ecol Evol. 2018;00:1–13. h t tp s : //d o i .
org /10.1002/ece3.433 3
... Whip spiders (Amblypygi Thorell, 1883), an order of tropical arachnids related to spiders (Weygoldt, 2000), which reach their greatest diversity in the Mexican Neotropics (Armas, 2006;Harvey, 2003), offer a model system to address the drivers of tropical diversification. Unlike spiders, most of which are capable of dispersal on air currents (Weyman, 1993), whip spiders are limited to walking and possibly rafting (Chapin et al., 2018). Their vagility is further constrained by an ecological requirement for humidity, which restricts them to forests, caves or the vicinity of permanent water sources in arid areas (Weygoldt, 2000). ...
... Their vagility is further constrained by an ecological requirement for humidity, which restricts them to forests, caves or the vicinity of permanent water sources in arid areas (Weygoldt, 2000). Although phylogeographical studies of whip spiders remain scarce, the few published to date confirm that their diversity is underestimated and informative for understanding diversification in the tropics (Chapin et al., 2018;Esposito et al., 2015;Prendini et al., 2005;Reveillion et al., 2020). ...
... The ingroup comprised 26 specimens of Acanthophrynus from 16 localities (a proxy for populations), covering most of the distribution ( (Weygoldt, 2000). cytochrome c oxidase subunit I (COI), were selected for efficacy in reconstructing the phylogeny of whip spiders (Chapin et al., 2018;Esposito et al., 2015;Harrison et al., 2017;Prendini et al., 2005). Loci were amplified using universal primers and/or, in the case of COI, 28S ...
The tropics contain many of the most biodiverse regions on Earth but the processes responsible for generating this diversity remain poorly understood. This study investigated the drivers of diversification in arthropods with stenotopic ecological requirements and limited dispersal capability using as model the monotypic whip spider (Amblypygi) genus Acanthophrynus, widespread in the tropical deciduous forests of Mexico. We hypothesized that for these organisms, the tropical deciduous forests serve as a conduit for dispersal, with their disappearance imposing barriers. Given that these forests are located in a region of complex geological history and fluctuated in extent during the Pliocene-Pleistocene glacial/interglacial cycles we couple molecular clock dating, paleoclimatic niche modeling and ancestral area reconstruction to test if and how habitat fragmentation promoted diversification in Acanthophrynus. Concomitant with the expected role of landscape change, we demonstrate that orogeny of the Trans-Mexican Volcanic Belt, in the Late Miocene/Early Pliocene (6.95-5.21 mya), drove the earliest divergence of Acanthophrynus through vicariance. Similarly, as expected, the later onset of glaciations strongly impacted diversification. Whereas a more stable climate in the southern part of the distribution enabled further diversification, a marked loss of suitable habitat during the glaciations only allowed dispersal and diversification in the north to occur later, resulting in a lower overall diversity in this region. Importantly, barriers and diversification patterns identified in Acanthophrynus are reflected in the phylogeography of codistributed vertebrates and arthropods, emphasizing the profound impact of Trans-Mexican Volcanic Belt orogeny and glacial/interglacial cycles as drivers of diversification in the Mexican Neotropics.
... Geographical distance is the obvious explanation for genetic divergences (see also [67]). For example, only two species were both found on the mainland (Florida) and on an island. ...
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Islands—whether classic oceanic islands or habitat islands such as isolated thermal vents, mountain tops, or caves—often promote the diversification of lineages that colonize them. We examined CO1 mtDNA sequence divergences within the tailless whip spider genus Phrynus Lamarck, 1809 (Amblypygi: Phrynidae) among oceanic islands and among cave ’islands´ distributed across the Caribbean archipelago and on the continental mainland. The significance of this study lies in the extensive taxon sampling of a supposedly depauperate lineage (considering its age), over a large proportion of its geographical range, and the discovery of deep mtDNA sequence divergences. We sampled thousands of specimens—and sequenced 544, including six outgroup species—across 173 localities on 17 islands (135 localities) and five countries on the North to South American mainland (38 localities), including a total of 63 caves. Classical taxonomy identified ten named Phrynus and two Paraphrynus Moreno, 1940 species. Paraphrynus seems to be paraphyletic and nested in Phrynus. Uncorrected genetic distances within named species and among morphological species ranged up to 15% and 19%, respectively. Geographic distances explained a significant portion of genetic distances on islands (19%, among both subterranean and epigean specimens), and for epigean specimens on the mainland (27%). Species delimitation analyses indicated that the 12 named species harbored from 66 to well over 100 putative species. The highest number of species was indicated by the GMYC method (114 species) while the Bayesian Poisson tree processes (bPTP) and the BP&P relaying on the Markov chain Monte Carlo Bayesian Phylogenetic model estimated an upper level of 110 species. On the other hand, the recently recommended and relatively conservative distance-based (phylogeny free) ASAP model has the greatest support for 73 species. In either case, nearly all putative species are tightly limited to a single locality, often a small cave system, and sometimes to the surrounding epigean area. Caribbean Phrynus diversity has likely been vastly underestimated, likely due to both morphological crypsis and the ignorance of Caribbean cave fauna. Although mtDNA sequences can suggest species limits, nuclear DNA sequencing and detailed morphological research are necessary to corroborate them and explore whether this phenomenon constitutes species radiation or perhaps just mtDNA divergences as a consequence of, for example, stationary females and actively dispersing males.
... Heterophrynus species could be, and how much of this potential distribution is part of an already established protected area. At the moment, only a paper about the potential distribution of species of Phrynidae has been published, however, it refers to a species of Phrynus from the Caribbean Islands (Chapin et al., 2018). So this is also the first paper about niche ENM in Heterophrynus. ...
Full-text available
The species Heterophrynus boterorum is endemic to Colombia, and was described in 2013 with just a few specimens. It has morphological variation that may be correlated with environmental conditions, or with isolation processes. We modeled the potential distribution of this species using software Maxent in order to know of other possible occurrence localities and the influence of environmental variables which can condition its presence. Additionally, we contrasted the potential distribution with the National System of Protected Areas of Colombia. The species has a potential distribution in the central region of the Andes in the Cordillera Central and Occidental, which connects all known populations. Precipitation and temperature, especially during the driest season, were the most influential variables in the model, which is coherent regarding the requirements for humidity and climatic stability in Amblypygi. Only one of the known populations is recorded in a protected area, so it is necessary to design better conservation strategies to preserve H. boterorum.
... This can be exemplified in the hardwood hammock habitats of P. marginemaculatus. Odor plumes present within the Florida Keys and the Everglades environments, which experience occasional strong winds (Chapin et al., 2018;Greller, 1980), should be more continuous with lower peak concentrations because of lower overall turbulence levels (Justus et al., 2002;Moore and Crimaldi, 2004;Murlis, 1997). Conversely, more complex rainforests, such as the habitats of P. laevifrons in Costa Rica, will have reduced wind velocity and a greater number of elements producing flow eddies resulting in odor stimuli that are more heterogeneous (Chapin and Hebets, 2016;Chazdon et al., 2010;Lawton and Putz, 1988;Moore and Crimaldi, 2004;Wiegmann et al., 2016;Wilson et al., 1985). ...
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Recent improvements in genetic analyses have paved the way in using molecular data to answer questions regarding evolutionary history, genetic structure, and demography. Key deer are a federally endangered subspecies assumed to be genetically unique, homogeneous, and have a female-biased population of approximately 900 deer. We used 985 bp of the mitochondrial cytochrome b gene and 12 microsatellite loci to test two hypotheses: (1) that Key deer are isolated and have reduced diversity compared to mainland deer and (2) that isolation of the Florida Keys has led to a small population size and a high risk of extinction. Our results indicate that Key deer are indeed genetically isolated from mainland white-tailed deer and that there is a lack of genetic substructure between islands. While Key deer exhibit reduced levels of genetic diversity compared to their mainland counterparts, they contain enough diversity to uniquely identify individual deer. Based on genetic identification, we estimated a census size of around 1000 individuals with a heavily skewed female-biased adult sex ratio. Furthermore, our genetic and contemporary demographic data were used to generate a species persistence model of the Key deer. Sensitivity tests within the population viability analysis brought to light the importance of fetal sex ratio and female survival as the primary factors at risk of driving the subspecies to extinction. This study serves as a prime example of how persistence models can be used to evaluate population viability in natural populations of endangered organisms.
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Arachnologists have uncovered tantalizing details about amblypygid behavioral ecology—the study of the fitness consequences of their behavior. Thus, it is the aim of this review to position Amblypygi as a useful system in which to investigate the principles of animal behavioral ecology. We synthesize amblypygid habitat preference and navigation modalities; predator, prey, parasite, parasitoid, cannibal, and commensal interactions; resource contests and territoriality; mating systems and mate choice; parental investment and sociality; and genetics and genomics as they relate to behavioral ecology. We present ideas for future research in each of these areas and discuss future directions for Amblypygi behavioral ecology research as they relate to four areas of behavioral ecology: adaptation, evolutionary history, mechano-sensory control of behavior, and behavioral development. We conclude by identifying several avenues of Amblypygi behavioral ecology that we think have the highest potential for transformative discoveries.
Aim To synthesize the species distribution modelling (SDM) literature to inform which variables have been used in MaxEnt models for different taxa and to quantify how frequently they have been important for species’ distributions. Location Global. Methods We conducted a quantitative synthesis analysing the contribution of over 400 distinct environmental variables to 2040 MaxEnt SDMs for nearly 1900 species representing over 300 families. Environmental variables were grouped into 24 related factors and results were analysed by examining the frequency with which variables were found to be most important, the mean contribution of each variable (at various taxonomic levels), and using TrueSkill™, a Bayesian skill rating system. Results Precipitation, temperature, bathymetry, distance to water and habitat patch characteristics were the most important variables overall. Precipitation and temperature were analysed most frequently and one of these variables was often the most important predictor in the model (nearly 80% of models, when tested). Notably, distance to water was the most important variable in the highest proportion of models in which it was tested (42% of 225 models). For terrestrial species, precipitation, temperature and distance to water had the highest overall contributions, whereas for aquatic species, bathymetry, precipitation and temperature were most important. Main conclusions Over all MaxEnt models published, the ability to discriminate occurrence from reference sites was high (average AUC = 0.92). Much of this discriminatory ability was due to temperature and precipitation variables. Further, variability (temperature) and extremes (minimum precipitation) were the most predictive. More generally, the most commonly tested variables were not always the most predictive, with, for instance, ‘distance to water’ infrequently tested, but found to be very important when it was. Thus, the results from this study summarize the MaxEnt SDM literature, and can aid in variable selection by identifying underutilized, but potentially important variables, which could be incorporated in future modelling efforts.
This book had its origin when, about five years ago, an ecologist (MacArthur) and a taxonomist and zoogeographer (Wilson) began a dialogue about common interests in biogeography. The ideas and the language of the two specialties seemed initially so different as to cast doubt on the usefulness of the endeavor. But we had faith in the ultimate unity of population biology, and this book is the result. Now we both call ourselves biogeographers and are unable to see any real distinction between biogeography and ecology.