Integration of global fossil and modern biodiversity data reveals dynamism and stasis in ant ...

107 Pages·2015·5.49 MB·English

JournalofBiogeography(J.Biogeogr.)(2015)
Integration of global fossil and modern
ORIGINAL
ARTICLE biodiversity data reveals dynamism and
stasis in ant macroecological patterns
Benoit Gu(cid:1)enard1,2*, Vincent Perrichot3 and Evan P. Economo1,4
1OkinawaInstituteofScienceandTechnology ABSTRACT
GraduateUniversity,Onna-son,Okinawa
Aim We investigate the dynamics of ant biodiversity patterns and community
904-0495,Japan,2SchoolofBiological
structure from the Eocene until the present. Our goal is to empirically test
Sciences,TheUniversityofHongKong,Pok
hypotheses regarding the similarities in composition and structure of fossil and
FuLamRoad,HongKongSAR,China,
3CNRSUMR6118 G(cid:1)eosciences,Universit(cid:1)ede modern ant faunas to understand the historical processes influencing modern
global biodiversity patterns.
Rennes1,RennesCedex35042,France,
4DepartmentofEcologyandEvolutionary Location Global.
Biology,UniversityofMichigan,AnnArbor
MI48104,USA Methods We integrated two recently developed databases of the geographical
distributions of fossil and modern ant genera and analysed the evolution of
diversityandcompositionsincetheEocene,c. 55 Ma.Weassembledathirdnew
database on community structure of ants, and used it to compare community
structureoffossilassemblageswithmoderncommunitiesindifferentbioregions.
Results The analyses of generic composition and community structure were
congruent, supporting a strong affinity between the Western Palaearctic ant
fauna and modern Indomalayan and Australasian assemblages, and of a wide-
spread Holarctic ant palaeofauna, and affinity between fossil Caribbean and
modern Neotropical faunas. In addition, neither generic composition nor com-
munity structure of fossil assemblages showed evidence of taphonomic bias
towards arboreal taxa.
Main Conclusions The aggregated fossil record reveals the dynamic nature of
macroecological patterns in ant biodiversity during the Cenozoic, with conti-
nental-scale generic extinctions common and important in shaping modern ant
assemblages. Our results suggest major compositional changes for the Western
Palaearctic bioregion and the Caribbean bioregions. The ant palaeofauna of the
Western Palaearctic bioregion was then very similar in composition and struc-
ture to the one observed now in the Indomalayan bioregion, supporting the
notion that modern-day ‘tropical’ biomes were historically much more wide-
spread, while temperate biotas are more recently evolved. Our results under-
score the importance of a palaeogeographical perspective in understanding
modern-day macroecological patterns.
*Correspondence:BenoitGu(cid:1)enard,Schoolof Keywords
BiologicalSciences,TheUniversityofHong Cenozoic, community structure, extinctions, Formicidae, fossils, generic
Kong,PokFuLamRoad,HongKongSAR,
diversity, global diversity patterns, historical biogeography, neofauna, palaeo-
China.
fauna.
E-mail:[email protected]
efforts have been bolstered by new informatic tools allowing
INTRODUCTION
for aggregations of vast amounts of data. As noted by
Biologists have long strived to understand the macroecologi- others (Manchester et al., 2009; Jones & Safi, 2011), the
cal patterns such as the latitudinal diversity gradient and large-scale biodiversity patterns we observe today are an
the distribution of Earth’s biomes. In recent years, these outcome of a long and dynamic evolutionary history driven
ª2015JohnWiley&SonsLtd http://wileyonlinelibrary.com/journal/jbi 1
doi:10.1111/jbi.12614
B.Gu(cid:1)enard et al.
by climatological, geological and ecological shifts. The towards certain habitats or strata. We first review large-scale
aggregation and synthesis of fossil data is critical for resolv- ant biogeography to establish some context and hypotheses
ing the temporal dimension of biodiversity dynamics and for ouranalysis.
understand the processes driving patterns.
While data syntheses have advanced rapidly for vertebrates
Background and hypotheses
and plants, invertebrates lag behind despite constituting the
large majority of the global diversity. Among invertebrates, Recent work on ant evolution including molecular phyloge-
ants are one of the most ecologically dominant and well- netic analyses (Brady et al., 2006; Moreau et al., 2006; Mor-
studied groups. Understanding the mechanisms and the eau & Bell, 2013), diversification hypotheses (Wilson &
pathways by which this group achieved such ecological and Ho€lldobler, 2005; Moreau et al., 2006; Perrichot et al.,
evolutionary success represents a major endeavour. Recently, 2008b), and new description of ancient fossils nearly 100 Ma
a global database on the distribution of modern ant genera old (Nel et al., 2004; Perrichot et al., 2008a; Barden & Gri-
was compiled revealing large-scale patterns in richness and maldi, 2012), indicate that all the genus-level taxa known
composition (Gu(cid:1)enard et al., 2012). Work on fossil ants has from the first 50–60 Myr following their first appearance are
mainly focused on taxonomic analysis of individual speci- now extinct. The rise of the modern ant fauna is a more
mens (e.g. Baroni Urbani, 1980; Perrichot et al., 2008a; recent phenomenon occurring probably during the early
Dlussky & Wedmann, 2012). Only a few synthetic analyses Cenozoic and continuing until the present (Brady et al.,
existonparticulardepositswitharichantpalaeocommunity, 2006; Moreau et al.,2006; LaPollaet al., 2013).
such as Baltic and Dominican ambers (Wheeler, 1915; Wil-
son, 1985; Dlussky & Rasnitsyn, 2009; Dlussky & Putyatina,
The Fossil West Palaearctic–Modern Indomalayan-
2014). Recently, a world catalogue of fossil ants was com-
Australasian Affinity
piled (Perrichot, 2014), and the updated global fossil record
was reviewed (LaPolla et al., 2013). However, our macro- One of the pioneering -and still most impressive- studies on
scopic view of ant biodiversity, across all genera and across fossil ants to-date was conducted by Wheeler (1915) on 9527
theglobe, remains firmlyrootedinthepresent. ant specimens from Eocene (37–42 Ma) Baltic amber.
Here, for the first time, we assemble a comprehensive Wheeler noted then that modern American and African ele-
global database of ant genera known both from fossil and ments are nearly completely missing from Baltic amber, and
modern species, providing relevant historical context to the he described this ant palaeofauna as a ‘mixture of what at
patternsobservedinextantgenericdistributions.Weevaluate the present day we are able to recognize as at least four dif-
the extent to which historical assemblages of genera resemble ferent faunas, the Palaearctic, the Indian, the Malayan and
modern faunas, both in the same and in distant geographical the Australian, with a little more than ⅓ of the genera and
regions. We use these data on generic composition to evalu- nearly ½ of the species Palaearctic and the reminder belong-
ate biogeographical hypotheses developed to explain modern ing to Indomalayan and Australian types’ (Wheeler, 1915, p.
ant composition patterns. 12). Wheeler’s observations and conclusions followed those
While generic composition varies in informative ways of Emery (1892), who previously noticed the strong affinity
across major bioregions, the distribution of diversity at of much smaller sample of Sicilian amber ant fossils with the
higher taxonomic levels also varies in important ways that modern Indo-Australian fauna. However, these authors ver-
are not captured by the presence–absence of genera. For bally described patterns but did not test them quantitatively.
example, compared with faunas in other continents, both Furthermore, as those original studies, subsequent work has
local and regional ant faunas of Australia are much more enriched our understanding of both the fossil and modern
dominated by species of the subfamily Dolichoderinae than ant faunal distributions, with studies on new deposits avail-
other regions. These broad differences in community organi- able (Europe: Dlussky & Rasnitsyn, 2009; Dlussky & Wed-
zation also help us interpret the organization of historical mann, 2012; Dominican amber: Wilson, 1985; Baroni
ant assemblages. Likewise fossil records may be biased Urbani, 1995; Chiapas: Solo(cid:1)rzano Kraemer, 2007), and
towards ants living in certain habitats (forest, open, etc.) and improvements in taxonomy of both modern and fossil taxa
in different ecological strata (arboreal, epigaeic, hypogaeic) (Ward, 2007). The aggregation of the most recent data for
as noted for instance by Dlussky et al. (2009) on the domi- both the fossil and modern ant distributions (Gu(cid:1)enard et al.,
nanceofarborealantindividualsintheOligoceneBembridge 2010; Perrichot, 2014) allow now for more rigorous compar-
Marls deposits. ison oftheaffinities between thosedifferent assemblages.
To compare community organization of fossiland modern
assemblages, we compiled a global database of modern ant
The East Palaearctic–East Nearctic Disjunction
community structure from all major biomes and habitat
types, as characterized by the distribution of species richness Forover 150 years, plant ecologists havenoticed strongsimi-
across subfamilies. Using this data set, we evaluated whether larities between plant communities found in East Asia and
the organization of fossil communities resembles any mod- East North America, both sharing similar genera, while those
ern-day faunas, and if there is evidence of a taphonomic bias were absent from Europe or West America (Wen, 1999).
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Historical biogeographyof ants
Those observations led to the hypothesis that during most of However, such patterns may be influenced by taphonomic
the Cenozoic a large mixed mesophytic forest covered the bias. Several studies of European fossil deposits found that
Northern Hemisphere (Tiffney, 1985; Manchester, 1999; the abundance and richness of ant species from the subfam-
Greenwood et al., 2005), with the North Atlantic and Bering ily Dolichoderinae in ant communities was much higher
land bridges connecting Eurasia and North America facilitat- than usually observed in modern communities (Wheeler,
ing transcontinental dispersal of plant and animal lineages. 1915; Dlussky & Rasnitsyn, 2002; LaPolla et al., 2013). This
By the late Tertiary and during the Quaternary, major cool- led these authors to suggest that because modern Doli-
ing events provoked massive extinctions in Europe and part choderinae are most commonly arboreal, the taphonomy of
of the Nearctic bioregion (Tiffney, 1985) and closed overland amber fossilization could be biased towards arboreal species.
dispersal routes. Despite support from numerous plants and However, more general palaeoecological studies have shown
vertebrate studies (Tiffney, 1985; Manchester, 1999; San- that a significant fraction of organisms embedded in amber
martin et al., 2001), this hypothesis has received less atten- were representatives of the litter and low vegetation of the
tion for entire communities of insects groups (but see Von forest (Henwood, 1993; Perrichot, 2004). Thus, it is possible
Dohlen et al., 2002). If valid, we predict that the fossil ant that it is the preponderance of Dolichoderines on other sub-
assemblages known from the Holarctic bioregion (East family-level taxa which (according to the hypothesis
Palaearctic, West Palaearctic and Nearctic bioregions) should described above) may reflect similarities to modern Indoma-
be aligned with the current faunas of the Eastern Asian and layan and Australasian faunas. In contrast, if the taphonomy
Eastern Nearctic bioregions. Alternatively, regions that were of ant fossils is biased towards arboreal taxa, then we should
affected by extinctions should present limited affinities find greater affinities with community structure found in
between their Palaeo-and Neofauna. contemporary arboreal communities, but not particularly
allied withagiven bioregion.
To summarize, in this study we use three recently devel-
Similarity between the current Neotropical bioregion and
oped databases to address the following goals. (1) By com-
the Miocene Caribbean fauna
paring past and modern distributions of ant genera, we
A comparison of the Hispaniolan modern fauna and palaeo- explore the validity of multiple biogeographical hypotheses
fauna conducted by Wilson (1985) showed the similarity of developed to explain modern ant composition patterns,
the past Dominican amber ant fauna with the current ant namely (i) the fossil West Palaearctic ant fauna affinity with
fauna of the Neotropical bioregion. A similar pattern with the modern Indomalayan-Australasian fauna, (ii) the East
moderate similarity between modern and palaeo-Hispaniolan Nearctic–East Palaearctic disjunction, and (iii) the fossil Car-
fauna, and strong similarities between palaeo-Hispaniolan ibbean affinity with the modern Neotropical fauna. (2) We
and modern South and North American fauna has been study the relative species richness of ant subfamilies within
observed in several groups of insects (Solo(cid:1)rzano Kraemer, communities present in multiple modern bioregions and
2007)and spiders (Penney, 2008).Incontrast, Baroni Urbani habitats in order to characterize the structural affinities of
and de Andrade highlighted examples of Dominican fossils European fossil assemblages of the Palaeogene period. (3)
that had strong affinities with extant Old World ant fauna, We test the hypothesis that the generic representation and
in particular the current Australasian taxa (Baroni Urbani, community structure within the European fossil record is
1980, 1995; Baroni Urbani & de Andrade, 2003), a pattern biasedtowards anover-representation of arborealspecies.
also observed occasionally in other insect groups (Grimaldi
et al.,2013).Weuseourdatatoevaluatetheextent towhich
METHODS
the Caribbean ant palaeofauna is related to the Neotropical
faunaversus faunasof other bioregions.
Fossil generadatabase
We focusedon ant generaknown from both thefossilrecord
Community organization across bioregions
and the modern ant fauna, as these provide information
In addition to the presence–absence of genera, other aspects about affinities between historical and extant faunas. Fossils
of community organization exhibit biogeographical variation. ofantswereassignedtospecificdeposits representing agiven
In ant assemblages, the relative proportion of the species area and a specific geological period. We assigned each
from the different subfamilies varies at both local and large deposit to a bioregion in order to compare generic fossil and
scales, and across habitat strata. In tropical forests, stratifica- modern ant records. Table S1 (see Appendix S2 in Support-
tion among microhabitats are well documented, with few ing Information) presents the main geological deposits where
overlaps between species inhabiting the arboreal stratum and ants have been collected and the bioregions and periods to
those living on the ground surface or deeper in the leaf litter which they were assigned. Controversial fossil records were
(Wilson, 1959; Bru€hl et al., 1998). At a continental-scale, excluded (seedetails inAppendix S1).
Ward (2000) briefly described major geographical differences Nine bioregions were considered in this study: the West
in how species richness is partitioned among subfamilies in Palaearctic, East Palaearctic, Indomalayan, Australasian,
leaf-litter assemblages. Afrotropical, Malagasy, Nearctic, Caribbean and the
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B.Gu(cid:1)enard et al.
Neotropical bioregion (see Appendix S1). Figure S1 in (Dlussky & Rasnitsyn, 2009). Our null hypothesis considers
Appendix S2 presents how the political regions used that all else equal, the proportion of genera known from
in Gu(cid:1)enard et al. (2012) were assigned to each bioregion. In each category (arboreal, epigaeic, hypogaeic) should be equal
order to evaluate the similarity between the ant fossil fauna if unbiased towards one category. The tested hypothesis here
of the Dominican amber with other bioregions, we consid- is that the proportion of genera known to live within each
ered the Caribbean as its own bioregion. This choice was stratum does not show a bias towards a specialized habitat
motivated by the results of previous studies on the dissimi- life style. This represents the simplest hypothesis to show
larity between the modern and the Dominican ant palaeo- that all strata-inhabitants could be preserved in fossilization
fauna(Wilson, 1985;Baroni Urbani, 1995). processes. We used a chi-square analysis to test this hypothe-
sis both including and excluding alate individuals from the
records.
Community database
Using our databases of fossil and extant community com-
To compare the community structure of fossil and modern position, we asked if fossil assemblages resemble any extant
ant assemblages, we built a database from 1060 publica- communities somewhere on the globe (bioregion, habitat,
tions, providing species composition at local and regional and ecological stratum) based on the distribution of richness
scales. Species richness for each of the 16 extant ant sub- across subfamilies. We took two approaches to answering
families was extracted, and the relative proportion of spe- this question. First, we used nonmetric multidimensional
cies richness (number of species in a subfamily/total species scaling (NMDS) to characterize the variability in community
richness collected) was calculated. Other relevant data, such composition within and across bioregions, and place the fos-
as spatial coordinates, elevation, habitat type, collection sil communities in this context. Second, we used a multino-
techniques and target strata (hypogaeic, epigaeic, arboreal mial regression approach to statistically assess which modern
or any combination of those) were also noted. After filter- faunasmost closely resemblethefossil data.
ing the sites due to certain criteria (see Appendix S1), 1736
sites representative of modern communities were used for
Ordinations
the analysis. Details on the number of sites within each
bioregion and for each habitat are given in Table S2 in Nonmetric multidimensional scaling and related ordination
Appendix S2. techniques take high dimensional data and arrange it in a
Modern ant assemblages were compared to the fossil low-dimensional form where distance between points in the
assemblages of the Baltic, Bitterfeld, Rovno and Scandinavian low dimensional space is representative of distance in the
amberdeposits compiled byDlussky &Rasnitsyn (2009) rep- higher dimensional space. We performed this analysis to
resenting over 16,700 inclusions (respectively Baltic = 14,915, visualize where the fossil communities fall in the context of
Bitterfeld = 1039; Rovno = 501; and Scandinavian = 271). the extant communities. We first calculated the proportion
Similar species-level data were not readily available for other of the species richness found in each subfamily. We then cal-
deposits. For this analysis, all taxa, independently of their culated the Euclidean distance between all community pairs,
status of extinct or extant, were included in the fossil ant and performed a 2-dimensional NMDS using Matlab and
community assessment. thesum ofsquareddistance asthestress criterion.
Analyses Multinomial logistic regression analysis
To evaluate affinities between historical and modern biore- We used multinomial logistic regression to fit a model for
gions, we calculated the fraction of genera present in each community composition (distribution of species richness
fossildepositthatarealsopresentintheextantfaunaofeach across subfamilies), using bioregion, habitat type, and stra-
bioregion, considering only those genera from the fossil tum as predictor variables. Then, using the models fitted to
record that arestillextant somewhereintheworld. extant communities, we ask which one best predicts the
To evaluate taphonomic bias based on generic composi- observed composition of the fossil assemblage. The model
tion, we classified the extant genera known from the fossil predicts the vector of frequencies across each subfamily, and
records into one of the following categories: arboreal, epi- a community of k species is treated as a multinomial draw k
gaeic, hypogaeic, arboreal + epigaeic, epigaeic + hypogaeic, times from that generating distribution. This multinomial
arboreal + epigaeic + hypogaeic (no genera were classified as regression approach accounts for the noise introduced by
arboreal + hypogaeic). Furthermore, we considered if the sampling effects in low richness sites (due either to actual
fossil specimens for each genus were known as worker (non- low richness or undersampling), thus we could include low
flying individual) or alate (flying gyne or male). This is an richness sites giving us a total of 1736 communities in the
important consideration as most compression fossils analysis.
(through sedimentation in water) are represented by alate We coded the nine bioregions and four habitat types as
individuals and many hypogaeic species are over-represented binary indicator variables in the analysis. For the three strata
by alate individuals trapped in resin during mating flights (ground, arboreal, hypogaeic), some sampling efforts focused
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Historical biogeographyof ants
on more than one stratum. For those we used a dummy Caribbean bioregion (83%). Other bioregions present less
coefficient of either 1/2 if two of the three were used or 1/3 affinity with the fossil fauna of the Nearctic bioregion (39–
if all three were used. In this way we let some community 57%). Those values differ, however, for the two geological
samples be a mixture of different strata. After fitting the periods considered. The Nearctic Eocene fauna presents
model to the extant community data set, we used the fitted stronger affinities with the Eastern Palaearctic, the Indoma-
model to predict a probability vector for each combination layan and the Western Palaearctic bioregions (80% overlap
of predictors (each biome times each habitat type times all of generic composition for all; Fig. 1). In contrast, the over-
combinations of strata). We then calculated the likelihood of lap with the Caribbean bioregion is less pronounced (60%;
each multinomial model given each set of fossil data from Fig. 1). It is important tonote that thenumber offossil gen-
thefour deposits andallfossil datacombined. eraknownfromthisperiodislimited(n = 11).TheMiocene
fauna is comparable to the overall pattern described above
with, however, lower similarity values with the Eastern and
RESULTS
Western Palaearctic bioregions and the Indomalayan biore-
We gathered 227 unique fossil per period records for 74 ant gion, but with higher similarity value with the Caribbean
genera spread over 10 subfamilies, which represent c. 23% of bioregion.
all modern ant genera and 63% of modern ant subfamilies. The fossil fauna of the East Palaearctic is most aligned
Based on the age estimation given to each fossil deposit (see with the modern ant fauna of the Indomalayan bioregion
Table S1 in Appendix S2), 35, 25 and 64 genera are known (Fig. 1). The affinity of the fossil and modern ant fauna of
respectively from the Eocene, the Oligocene, and the Mio- the Eastern Palaearctic bioregion present strong affinities,
cene (see Fig.S2 inAppendix S2). with 83% of the genera known from the fossil records still
Within the set of the genera studied, the Caribbean and present in this bioregion. The overlap of the East Palaearctic
the Western Palaearctic bioregions were the most diverse fossil fauna with the modern Nearctic bioregion is also
with 47 and 39 fossil genera collected respectively (see noticeable (67%). However, the highest affinity between
Fig. S2 in Appendix S2). The Nearctic and the Eastern those two bioregions is found between the Eocene Nearctic
Palaearctic bioregions were less diverse with 25 and 12 fossil palaeofauna andthemodern EastPalaearctic fauna (80%).
genera collected respectively. The fossil records from the
Australasian, Afrotropical, Indomalayan, Malagasy or
Taphonomic biasof generic records
Neotropical bioregions for the periods considered were
scarce or totally absent. From 74 extant genera known also to have fossil species, our
results did not support the hypothesis that arboreal genera
were overrepresented in the fossil record (Table 1, n = 96,
Generic overlaps
v2 = 0.53, P = 0.77), even when considering only the genera
We evaluated the fraction of fossil genera of different biore- known from the worker caste (n = 66, v2 = 1.09, P = 0.58).
gions that are present in the modern faunas of those same Those results may be limited as many genera could not be
bioregions, using genera that are present in both time peri- associated to a strict category (arboreal, epigaeic or hypo-
ods. The palaeofauna of the West Palaearctic bioregion, for gaeic) as several of their extant species are known to occupy
all periods considered, shows its strongest overlap with the more than one stratum. The multinomial logistic regression
modern ant fauna of the Indomalayan, Eastern Palaearctic analysis (Table 2) supports an epigaeic origin of the species
and Australasian bioregions (95%, 90% and 79.5% of fossil richness across subfamilies when all fossil deposits sites are
genera are present in the modern faunas respectively). In considered. This result is, however, slightly different when
contrast, the fossil ant generic composition of the West fossil deposits are considered individually. While the Baltic
Palaearctic bioregion show limited overlap to its modern amber and Bitterfeld amber deposits relate more strongly to
equivalent, with only 64% of fossil genera occurring in mod- an epigaeic or epigaeic + hypogaeic origin, the Rovno and
ern faunas; a percentage similar to those observed in the Scandinavian amber deposits appear biased towards an arbo-
Nearctic (67%), Afrotropical (64%) or Neotropical biore- real community composition origin.
gions (64%). Overlap values are similar between the geologi-
calperiods considered (Fig. 1).
Community structure comparison
The Caribbean ant palaeofauna has the highest overlap
with the Neotropical and Nearctic bioregions (98% and 87% The clustering analysis shows that the different modern com-
similarity of genera respectively) and to a lesser extent with munities present a specific biogeographical signature that is
the modern Caribbean bioregion (74%). There is limited evi- translated in the relative presence and species richness of the
dence for overlap with other bioregions (52% to 37% simi- different ant subfamilies (Fig. 2). The fossil assemblages con-
larities, Fig. 1). sidered also strongly clumped together indicating important
The fossil fauna of the Nearctic bioregion shows its stron- affinities in their species composition at the subfamily level
gest affinity with its own modern fauna (100% overlap), the relative to modern assemblages. The fossil assemblages show
Neotropical bioregion (91%) and to a lesser extent with the particular affinities with modern communities of the
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Modern Ant Faunas
CarribeanNearcNtiecotropicaElthiopianMWaleagsta PsyalaEeaasrtc PtiaclaeaIrncdtioc-MalayaAnustralian
Carribean Miocene 0.74 0.87 0.98 0.43 0.39 0.37 0.43 0.52 0.50
Fossil Ant Nearctic Miocene 0.85 1.00 0.95 0.45 0.45 0.50 0.60 0.60 0.50
Faunas
Nearctic Eocene 0.60 1.00 0.80 0.30 0.30 0.80 0.80 0.80 0.40
East Palaearctic Miocene 0.42 0.67 0.67 0.33 0.42 0.67 0.83 1.00 0.75
Figure 1Genericsimilaritybetweentheant
West Palaearctic Miocene 0.40 0.65 0.60 0.50 0.45 0.65 0.90 0.95 0.75 palaeofaunaknownfromthedifferent
geologicalperiodsandthemodernant
West Palaearctic Oligocene 0.54 0.69 0.65 0.62 0.50 0.73 0.92 1.00 0.77 faunawithineachbioregion.Lightercolours
indicatehighersimilarities.Valuescanrange
West Palaearctic Eocene 0.52 0.71 0.65 0.58 0.45 0.68 0.90 1.00 0.74 from0(nogeneraincommon)to1(all
generaknownareshared).
Table 1Numberofantgeneraknowninthefossilrecordin Table 2Resultsofthemultinomiallogisticregressionanalysis
functionoftheknowncaste(workerorsexual)asfossilandthe presentingthespecificaffinitiesforallantfossildepositsand
microhabitattheypresumablyoccupied(basedoncurrent eachofthefourantfossildepositsstudiedwiththemodernant
ecologyofeachgenus). compositioninspeciesrichnessacrosssubfamiliesinfunctionof
theirorigin(bioregion),habitatandstrataofcollection.
Knownonly
Numberof Knownfrom fromsexual Nodata Likelihood
Genera workercaste caste available value Bioregion Habitat Strata
Arboreal 14 12 1 1 Allfossils (cid:1)152.906 Indomalaya Primaryforest E
Epigaeic 18 14 1 3 (cid:1)153.638 Australasia Primaryforest E
Hypogaeic 17 9 5 3 (cid:1)166.142 Australasia Primaryforest E+H
Epigaeicand 20 15 2 3 Baltic (cid:1)82.120 Indomalaya Primaryforest E
arboreal Amber (cid:1)87.315 Australasia Primaryforest E+H
Epigaeicand 1 0 1 0 (cid:1)89.854 Australasia Primaryforest E
hypogaeic Bitterfeld (cid:1)57.308 Australasia Primaryforest E
Allstrata 4 3 1 0 Amber (cid:1)58.419 Australasia Primaryforest E+H
(cid:1)60.256 Indomalaya Primaryforest E
Rovno (cid:1)17.409 Oceania Primaryforest A
Indomalayan, Australasian, and Neotropical bioregions
Amber (cid:1)17.532 Australasia Primaryforest A
(Fig. 2). The West Palaearctic modern ant communities are (cid:1)18.951 Indomalaya Primaryforest A
distinct from their fossil equivalent, a pattern also observed Scandinavian (cid:1)10.626 Oceania Primaryforest A
with modern Nearctic and East Palaearctic communities Amber (cid:1)11.367 Indomalaya Primaryforest A
(Fig. 2). (cid:1)12.421 Australasia Primaryforest A
The multinomial logistic regression analysis (Table 2)
A,arboreal;E,epigaeic;H,hypogaeic.
shows several consistent features among all fossil deposits
based on species richness across subfamilies. The structure of
fossilsdeposit communities isgenerally mostsimilartomod- generic level is one of the most noticeable features of the
ern communities in the Indomalayan and Australasian biore- data and analyses. For example, the generic extinction rates
gions. The Rovno amber and Scandinavian amber deposits of the Caribbean and Western Palaearctic bioregions follow-
also show some similarities with the modern assemblages in ing the Miocene period are at least 26% and 36% respec-
the Oceania bioregion. For all fossil deposits considered or tively. In addition, from 39 genera known from the
individually, themodel predictsaprimary forest origin. European deposits and with modern representatives some-
where in the world, 14 (or 36%) have gone extinct from this
bioregion or remain only in the southern portion of this
DISCUSSION
bioregion.
The aggregated fossil record reveals the dynamic nature of These numbers would undoubtedly increase significantly
macroecological patterns in ant biodiversity during the with the inclusion of genera only known from the fossil
Cenozoic. The commonness of large-scale extinctions on the record, which were excluded in our analysis. For example,
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Historical biogeographyof ants
Nearctic West Palaearctic East Palaearctic
Afrotropical Malagasy Oceania

2

s
i
x
A

S
D
M
N
Neotropical Indo-Malayan Australian
NMDS Axis 1
Figure 2Nonmetricmultidimensionalscalingofvariabilityinantspeciesrichnesscompositionacrosssubfamiliesinfunctionofthe
differentbioregionsoftheworld.Oneachfigure,fossildepositscommunitiesappearinred,moderncommunitiesforthespecific
bioregionappearinblueandingreytherestofthepointsnotspecifictothestudiedbioregion.Sizeofthedotisproportionaltothe
speciesrichnesswithbiggerdotsrepresentingrichercommunities.
extinct genera of the subfamily Aneuretinae are present in genera. For example the genus Perissomyrmex is only known
European Tertiary fossil deposits but the subfamily is cur- from a few localities in Central America and Southeast Asia
rently restricted to Sri Lanka (Dlussky, 2012). Similarly, (Ogata &Okido, 2007).
extinct ant genera of the subfamily Myrmeciinae are present
in Nearctic and European fossil faunas (Archibald et al.,
Thefossil West Palaearctic–modernIndomalayan-
2006), but the subfamily is now restricted to Australasia.
Australasian affinity
Regional extinction also occurred even within themost ubiq-
uitous ant genus, Camponotus (Gu(cid:1)enard et al., 2010), known Our analyses using several data sets and analytical
in the fossil record from England but now extinct in the Bri- approaches support the hypothesis of Emery (1892), and
tish Isles. This pattern of widespread, large-scale extinction Wheeler (1915) that the ant fauna of Europe during the
helps to explain some of the 20 extreme biogeographical dis- Eocene-Miocene has affinities with the Indomalayan biore-
junctions in ant genera observed today (Gu(cid:1)enard et al., gion and to a lesser extent the Australasian bioregion. In
2010), suggesting a broader historical distribution of those addition to the strong generic composition similarities, we
JournalofBiogeography 7
ª2015JohnWiley&SonsLtd
B.Gu(cid:1)enard et al.
also demonstrate a structural similarity in species richness of 2006).Thegenericcompositionofallthefossildepositsfrom
the extant subfamilies between the Cenozoic ant fauna of the Holarctic bioregion show high similarity with the current
Europe and the modern ant fauna of the Indomalayan and East Palaearctic or Indomalayan bioregions supporting the
Australasian bioregions. Without well-studied ant fossil hypothesis of a widespread ant assemblage in the Northern
records from the latter bioregions, it is difficult to determine Hemisphere possibly facilitated by intermittent land connec-
whether these cases represent contractions of a historically tions accessible to both cold and warm-adapted lineages (e.g.
wide-rangedgenera,orwhetherrangeshaveshiftedovertime Archibald et al., 2011). As discussed above, the overlap
into new bioregions. Studies conducted on other organisms between the now-extinct West Palaearctic fauna and the
such as plants (Manchester et al., 2009) and bees (Michez currentAsian ant faunawasespecially important.
et al., 2009), have suggested the former. One open question
iswhetherthesimilarityofWestPalaearcticfaunaswithAus-
Similaritybetween thecurrent Neotropical bioregion
tralasia is mostly due to recent arrivals of Indomalayan lin-
andthe MioceneCaribbean fauna
eages, and thus the true historical similarity is with
Indomalaya. Although it is difficult to be conclusive with the Our results support Wilson’s conclusion that the Dominican
available data, of the 39 genera that were previously present palaeofauna has strongest affinities with current Neotropical
in the West Palaearctic and are now restricted to the Indo- faunas. From 47 genera known from the fossil records of
malayan or Australasian bioregions, most (30) are present in Dominican amber, only one genus, Leptomyrmex, is not
both Indomalaya and Australasia. Eight are restricted to encountered in the Neotropical bioregion, and six genera are
Indomalaya, and only one isrestricted toAustralasia. Further unknown from the modern Nearctic. Leptomyrmex remains
study, including consideration of the phylogenetic positions an enigmatic case. A recent molecular phylogeny of the Doli-
of different genera and the ages of colonization events, could choderines (Ward et al., 2010)indicated that thesister group
more rigorously addressthis question. to Leptomyrmex is Neotropical, lending credence to the idea
Our analyses of community structure, the distribution of that a lineage colonized Australasia from the Neotropics and
species richness across subfamilies, also support an affinity gave rise to the current genus. However, Dlussky et al.
between the Western Palaearctic palaeofauna and modern (2014) recently argued based on morphology that the
Indomalayan and Australasian ant fauna. First, the four fossil Neotropical Leptomyrmex was nested within Old World Lep-
assemblages used in this study present strong similarities as tomyrmex. Further work is needed to better understand this
shown in the clustering analysis (Fig. 2). Second, fossil enigma. Additionally, although subgeneric patterns are not
assemblages show higher affinities with the modern commu- the focus of our analysis, recent work sheds light on a
nities observed in the Indomalayan and Australasian biore- prominent example in the genus Pheidole that influenced
gions (Fig. 1). Finally, these results are also supported by the Baroni Urbani’s conclusions (Baroni Urbani, 1995). The
modelling approach where fossil assemblages from the West presence of highly spinescent Pheidole (e.g. P. primigenia) in
Palaearctic bioregion are best predicted by models represent- the Dominican amber has been interpreted as presence of a
ing theIndomalayan orAustralasian bioregions (Table 2). lineage that is now restricted to the Old World, as all extant
Interestingly, the affinity of the European ant palaeofauna spinescent Pheidole are restricted to the IndoMalayan and
withthecurrent Afrotropical bioregion is verylimited. While Oceanian bioregions. However, recent phylogenetic analysis
seemingly counterintuitive based on the modern configura- of Pheidole (Sarnat & Moreau, 2011; Economo et al., 2015)
tion of continents, this could be explained by the separation showed that spinescence has evolved multiple times in the
of the African and Eurasian plates until the middle Miocene Old World, thus it seems likely that the spinescent forms in
period(McQuarrie et al., 2003). Dominican Pheidole reflect convergent evolution as intercon-
These results, based on three approaches, support the tinental dispersal and subsequent extinction, and such dis-
hypothesis that the fossil assemblages of Europe during the persal is otherwise exceedingly rare in Pheidole (Economo
Palaeogene were most similar in generic composition and et al.,2015).
community structure with the modern ant fauna of the
Indomalayan and Australasian bioregions. These results are
Taphonomic bias
also consistent with studies in other taxa, including (but not
limited to) Salticid spiders (Pro(cid:1)szn(cid:1)ski & Z_abka, 1980), bees Finally, our results indicate that ant fossil assemblages are
(Engel, 2001), Hemiptera (Popov et al., 2011), and plants not systematically biased towards arboreal communities. This
(Reid & Chandler, 1933; Manchester, 1999; Manchester result is supported both in terms of composition, where no
et al.,2009; Teodoridis et al., 2012). difference in the overall presence of hypogaeic-epigaeic-arbo-
real genera was retrieved, as well as in the subfamily compo-
sition in ant assemblages. Two fossils deposits, namely the
TheEast Palaearctic–EastNearctic disjunction
Rovno and the Scandinavian amber deposits, show modest
Support for the East Palaearctic–East Nearctic disjunction is support for a bias towards arboreal strata. It is unclear
common in plants and ferns (Wen, 1999), but scarcer for whether this reflects noise due to sampling effects or the
insects (for fossil examples, see Archibald & Makarkin, signal of real biological differences. Other comparisons
8 JournalofBiogeography
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Historical biogeographyof ants
between the Rovno and Baltic amber arthropods assemblages and B.G. were supported by OIST and an NSF grant to
showed that those deposits represent two different fauna, E.P.E. (NSFDEB-1145989).
with the Rovno amber fauna probably formed within a more
xeric subtropical forest (Perkovsky, 2009).
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