Journal of Biogeography (J. Biogeogr.) (2015)

ORIGINAL Integration of global fossil and modern ARTICLE data reveals dynamism and stasis in macroecological patterns Benoit Guenard1,2*, Vincent Perrichot3 and Evan P. Economo1,4

1Okinawa Institute of Science and Technology ABSTRACT Graduate University, Onna-son, Okinawa Aim We investigate the dynamics of ant biodiversity patterns and community 904-0495, Japan, 2School of Biological structure from the Eocene until the present. Our goal is to empirically test Sciences, The University of Hong Kong, Pok Fu Lam Road, Hong Kong SAR, China, hypotheses regarding the similarities in composition and structure of fossil and 3CNRS UMR 6118 Geosciences, Universitede modern ant faunas to understand the historical processes influencing modern Rennes 1, Rennes Cedex 35042, France, global biodiversity patterns. 4 Department of Ecology and Evolutionary Location Global. Biology, University of Michigan, Ann Arbor MI 48104, USA Methods We integrated two recently developed databases of the geographical distributions of fossil and modern ant genera and analysed the evolution of diversity and composition since the Eocene, c. 55 Ma. We assembled a third new database on community structure of , and used it to compare community structure of fossil assemblages with modern communities in different bioregions. 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 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: Benoit Guenard, School of Keywords Biological Sciences, The University of Hong Cenozoic, community structure, extinctions, Formicidae, fossils, generic Kong, Pok Fu Lam Road, Hong Kong SAR, diversity, global diversity patterns, historical biogeography, neofauna, palaeo- China. E-mail: [email protected] fauna.

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

ª 2015 John Wiley & Sons Ltd http://wileyonlinelibrary.com/journal/jbi 1 doi:10.1111/jbi.12614 B. Guenard 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 our analysis. 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 Holldobler,€ 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 -level taxa known composition (Guenard 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., exist on particular deposits with a rich ant palaeocommunity, 2006; Moreau et al., 2006; LaPolla et 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 the globe, remains firmly rooted in the present. 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 patterns observed in extant generic distributions. We evaluate 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 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: Solorzano Kraemer, 2007), and towards ants living in certain habitats (forest, open, etc.) and improvements in 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 (Guenard et al., nance of arboreal ant individuals in the Oligocene Bembridge 2010; Perrichot, 2014) allow now for more rigorous compar- Marls deposits. ison of the affinities between those different assemblages. To compare community organization of fossil and 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 For over 150 years, plant ecologists have noticed strong simi- 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).

2 Journal of Biogeography ª 2015 John Wiley & Sons Ltd Historical biogeography of 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 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 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 with a given 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 (Solorzano Kraemer, communities present in multiple modern bioregions and 2007) and spiders (Penney, 2008). In contrast, 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 biased towards an over-representation of arboreal species. also observed occasionally in other groups (Grimaldi et al., 2013). We use our data to evaluate the extent to which METHODS the Caribbean ant palaeofauna is related to the Neotropical fauna versus faunas of other bioregions. Fossil genera database

We focused on ant genera known from both the fossil record 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. of ants were assigned to specific deposits representing a given 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; Bruhl€ et al., 1998). At a continental-scale, excluded (see details in Appendix 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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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 Guenard 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- faunas most closely resemble the fossil 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 amber deposits compiled by Dlussky & 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. the sum of squared distance as the stress 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 fossil deposit that are also present in the extant fauna of each 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 are still extant somewhere in the world. 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

4 Journal of Biogeography ª 2015 John Wiley & Sons Ltd Historical biogeography of 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 to note that the number of fossil gen- the four deposits and all fossil data combined. era known from this period is limited (n = 11). The Miocene 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 in Appendix 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 and the modern East Palaearctic fauna (80%). genera collected respectively. The fossil records from the Australasian, Afrotropical, Indomalayan, Malagasy or Taphonomic bias of 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- cal periods 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

Journal of Biogeography 5 ª 2015 John Wiley & Sons Ltd B. Guenard et al.

Modern Ant Faunas West PalaearcticEast Palaearctic Indo-Malayan Neotropical Carribean Ethiopian Australian Nearctic Malagasy

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 1 Generic similarity between the ant West Palaearctic Miocene 0.40 0.65 0.60 0.50 0.45 0.65 0.90 0.95 0.75 palaeofauna known from the different geological periods and the modern ant West Palaearctic Oligocene 0.54 0.69 0.65 0.62 0.50 0.73 0.92 1.00 0.77 fauna within each bioregion. Lighter colours indicate higher similarities. Values can range West Palaearctic Eocene 0.52 0.71 0.65 0.58 0.45 0.68 0.90 1.00 0.74 from 0 (no genera in common) to 1 (all genera known are shared).

Table 1 Number of ant genera known in the fossil record in Table 2 Results of the multinomial logistic regression analysis function of the known caste (worker or sexual) as fossil and the presenting the specific affinities for all ant fossil deposits and microhabitat they presumably occupied (based on current each of the four ant fossil deposits studied with the modern ant ecology of each genus). composition in species richness across subfamilies in function of their origin (bioregion), habitat and strata of collection. Known only Number of Known from from sexual No data Likelihood Genera worker caste caste available value Bioregion Habitat Strata

Arboreal 14 12 1 1 All fossils À152.906 Indomalaya Primary forest E Epigaeic 18 14 1 3 À153.638 Australasia Primary forest E Hypogaeic 17 9 5 3 À166.142 Australasia Primary forest E+H Epigaeic and 20 15 2 3 Baltic À82.120 Indomalaya Primary forest E arboreal Amber À87.315 Australasia Primary forest E+H Epigaeic and 1010 À89.854 Australasia Primary forest E hypogaeic Bitterfeld À57.308 Australasia Primary forest E All strata 4 3 1 0 Amber À58.419 Australasia Primary forest E+H À60.256 Indomalaya Primary forest E Rovno À17.409 Oceania Primary forest A Indomalayan, Australasian, and Neotropical bioregions Amber À17.532 Australasia Primary forest A (Fig. 2). The West Palaearctic modern ant communities are À18.951 Indomalaya Primary forest A distinct from their fossil equivalent, a pattern also observed Scandinavian À10.626 Oceania Primary forest A with modern Nearctic and East Palaearctic communities Amber À11.367 Indomalaya Primary forest A (Fig. 2). À12.421 Australasia Primary forest 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 fossils deposit communities is generally most similar to mod- 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, the model predicts a primary 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,

6 Journal of Biogeography ª 2015 John Wiley & Sons Ltd Historical biogeography of ants

Nearctic West Palaearctic East Palaearctic

Afrotropical Malagasy Oceania NMDS Axis 2

Neotropical Indo-Malayan Australian

NMDS Axis 1

Figure 2 Nonmetric multidimensional scaling of variability in ant species richness composition across subfamilies in function of the different bioregions of the world. On each figure, fossil deposits communities appear in red, modern communities for the specific bioregion appear in blue and in grey the rest of the points not specific to the studied bioregion. Size of the dot is proportional to the species richness with bigger dots representing richer communities. 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., The fossil West Palaearctic–modern Indomalayan- 2006), but the subfamily is now restricted to Australasia. Australasian affinity Regional extinction also occurred even within the most ubiq- uitous ant genus, Camponotus (Guenard 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 (Guenard 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

Journal of Biogeography 7 ª 2015 John Wiley & Sons Ltd B. Guenard et al. also demonstrate a structural similarity in species richness of 2006). The generic composition of all the fossil deposits from 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-ranged genera, or whether ranges have shifted over time 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 current Asian ant fauna was especially important. et al., 2009), have suggested the former. One open question is whether the similarity of West Palaearctic faunas with Aus- Similarity between the current Neotropical bioregion tralasia is mostly due to recent arrivals of Indomalayan lin- and the Miocene Caribbean 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 is restricted to Australasia. 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 the sister group more rigorously address this 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 the Indomalayan or Australasian 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 with the current Afrotropical bioregion is very limited. 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 (Prosz nski & Zabka,_ 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 The East Palaearctic–East Nearctic 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 Journal of Biogeography ª 2015 John Wiley & Sons Ltd Historical biogeography of ants between the Rovno and Baltic amber assemblages and B.G. were supported by OIST and an NSF grant to showed that those deposits represent two different fauna, E.P.E. (NSF DEB-1145989). with the Rovno amber fauna probably formed within a more xeric subtropical forest (Perkovsky, 2009). While we cannot rule out the presence of taphonomic REFERENCES biases of various kinds based on these data alone, the lack of Archibald, S.B. & Farrell, B.D. (2003) Wheeler’s dilemma. a strong arboreal bias in amber fossilization is somewhat Acta Zoologica Cracoviensia, 46,17–23. non-intuitive. However, although resin is produced on the Archibald, S.B. & Makarkin, V.N. (2006) Tertiary giant trunks and branches of trees, it is also produced by roots at lacewings (Neuroptera: Polystoechotidae) revision and the ground level or underground (Martınez-Delclos et al., description of new taxa from western North America 2004), which in principle could catch soil-dwelling ants. and Denmark. Journal of Systematic Palaeontology, 4, Some amber deposits yield a large amount of such ‘litter 119–155. amber’ (Perrichot, 2004), providing fossils of litter-living Archibald, S.B., Cover, S.P. & Moreau, C.S. (2006) Bulldog organisms. ants of the Eocene Okanagan Highlands and history of the subfamily (: Formicidae: Myrmeciinae). An- CONCLUSIONS nals of the Entomological Society of America, 99, 487–523. Our results highlight the dynamic nature of biogeographical Archibald, S.B., Bossert, W.H., Greenwood, D.R. & Farrell, processes shaping modern ant assemblages. In particular, our B.D. 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In contrast, the Nearctic fossil genera that Cretaceous ant Haidomyrmex Dlussky (Hymenoptera: have not gone extinct are all still present in the Nearctic, with Formicidae), with two new species. American Museum 3755 – the exception of the subfamily Myrmeciinae which was in the Novitates, ,1 16. Nearctic and West Palaearctic during the Eocene and is now Baroni Urbani, C. (1980) The first fossil species of the Aus- restricted to Australasia (Archibald et al., 2006; Dlussky, 2012). tralian ant genus Leptomyrmex in amber from the Domini- The shift seen in Europe hints at a common explanation can Republic (Amber Collectio Stuttgart: Hymenoptera, € for the latitudinal diversity gradient; that tropical areas have Formicidae. III: Leptomyrmicini). Stuttgarter Beitrage zur 62 – been bigger for longer, whereas temperate areas are relatively Naturkunde Serie B, ,1 10. new biomes that may have not had time to build up diverse Baroni Urbani, C. 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In this context, we strongly Brady, S.G., Schultz, T.R., Fisher, B.L. & Ward, P.S. (2006) advocate for increased research in palaeoentomology. Further Evaluating alternative hypotheses for the early evolution work on existing deposits, and analysis of newly discovered and diversification of ants. Proceedings of the National 103 – fossil deposits in India (Cambay amber; Rust et al., 2010), Academy of Sciences USA, , 18172 18177. € Australia (Cape York amber; Hand et al., 2010), France (Oise Bruhl, C.A., Gunsalam, G. & Linsenmair, K.E. (1998) Stratifica- amber), and New Zealand, will no doubt enrich our knowl- tion of ants (Hymenoptera, Formicidae) in a primary rain for- 14 – edge of ant evolution and biogeography. est in Sabah, Borneo. Journal of Tropical Ecology, , 285 297. Dlussky, G.M. (2012) New fossil ants of the subfamily Myrmeciinae (Hymenoptera: Formicidae) from Germany. ACKNOWLEDGEMENTS Paleontological Journal, 46, 288–292. We warmly thank all the contributors to the Ant Genera of Dlussky, G.M. & Putyatina, T.S. (2014) Early Miocene ants the World Project who provided data to B.G. We thank (Hymenoptera, Formicidae) from Radoboj, Croatia. Neues three anonymous referees for comments on the ms. E.P.E. Jahrbuch fur€ Geologie und Pal€aontologie, 272, 237–285.

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Rust, J., Singh, H., Rana, R.S., McCann, T., Singh, L., Ander- Science, 229, 265–267. son, K., Sarkar, N., Nascimbene, P.C., Stebner, F., Thomas, Wilson, E.O. & Holldobler,€ B. (2005) The rise of the ants: a J.C., Solorzano Kraemer, M., Williams, C.J., Engel, M.S., phylogenetic and ecological explanation. Proceedings of the Sahni, A. & Grimaldi, D. (2010) Biogeographic and evolu- National Academy of Sciences USA, 102, 7411–7414. tionary implications of a diverse paleobiota in amber from the early Eocene of India. Proceedings of the National SUPPORTING INFORMATION Academy of Sciences USA, 107, 18360–18365. Sanmartin, I., Enghoff, H. & Ronquist, F. (2001) Patterns of Additional Supporting Information may be found in the animal dispersal, vicariance and diversification in the Holarc- online version of this article: tic. Biological Journal of the Linnean Society, 73, 345–390. Appendix S1 Supplementary methods and list of references Sarnat, E.M. & Moreau, C.S. (2011) Biogeography and mor- used to build the Global Ant Community Database. phological evolution in a Pacific island ant radiation. Appendix S2 Supplementary tables and figures. Molecular Ecology, 20, 114–130. Appendix S3 Data from the Global Ant Community Data- Solorzano Kraemer, M.M. (2007) Systematic, palaeoecology, base used for the global community analysis. and palaeobiogeography of the insect fauna from Mexican amber. Palaeontographica Abteilung A, 282,1–133. BIOSKETCHES Teodoridis, V., Kvacek, Z., Zhu, H. & Mazouch, P. (2012) Environmental analysis of the mid-latitudinal European Benoit Guenard is an assistant professor at the University Eocene sites of plant macrofossils and their possible ana- of Hong Kong. His research focuses on ant diversity patterns logues in East Asia. Palaeogeography, Palaeoclimatology, and the mechanisms that shape them at local to global 333–334 – Palaeoecology, ,40 58. scales. Tiffney, B.H. (1985) The Eocene North Atlantic land bridge: its importance in Tertiary and modern phylogeography of Evan P. Economo is interested in theoretical and empirical the Northern hemisphere. Journal of the Arnold Arboretum, approaches to understanding biodiversity patterns and pro- 66, 243–273. cesses in a geographical context. He is particularly fascinated Von Dohlen, C.D., Kurosu, U. & Aoki, S. (2002) Phylogenet- by the ecology, evolution, and biogeography of ants. ics and evolution of the eastern Asian-eastern North Vincent Perrichot is a palaeontologist interested in the American disjunct aphid tribe, Hormaphidini (Hemiptera: evolution of insects and the paleoecology of amber forests. 23 Aphididae). Molecular Phylogenetics and Evolution, , He is particularly fascinated by the origin and evolution of – 257 267. ants. Ward, P.S. (2000) Broad-scale patterns of diversity in leaf lit- ter ant communities. Ants: Standard methods for measuring Author contributions: E.P.E., B.G., and V.P. conceived the and monitoring biodiversity (ed. by D. Agosti, J.D. Majer, study. B.G. and V.P. collected the data, B.G. and E.P.E. anal- L.E. Alonso and T.R. Schultz), pp. 99–121. Smithsonian ysed the data. All authors contributed to the preparation of Institution Press, Washington. the manuscript. Ward, P.S. (2007) Phylogeny, classification, and species-level taxonomy of ants (Hymenoptera: Formicidae). Zootaxa, Editor: Lawrence Heaney 1668, 549–563.

Journal of Biogeography 11 ª 2015 John Wiley & Sons Ltd Journal of Biogeography

SUPPORTING INFORMATION

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

ant macroecological patterns

Benoit Guénard, Vincent Perrichot and Evan P. Economo

Appendix S2: Supplementary tables and figures

Table S1. List of fossil deposits where ant genera that have not gone extinct have been collected. The geological period and age of each deposit are taken from the Paleobiology

Database (https://paleobiodb.org). Bioregions are classified according to figure S1.

Deposit name Geological Estimated age Country / Recorded number period (Ma Years) Region of genera (Recent / Total) West Palaearctic bioregion Oise amber Early Eocene 52-55 France 9/11 Grube Messel, Darmstadt Middle Eocene 47 Germany 4/11 Eckfeld, Germany Middle Eocene 44 Germany 2/2 Baltic amber Middle Eocene 37- 42 Poland 28/51 Bournemouth, Dorset Middle Eocene 37-40 England 2/3 Scandinavian amber Late Eocene 34-42 Denmark 16/24 Celas, Gard Late Eocene 34-35 France 2/2 Isle of Wight Late Eocene 34 England 5/10 Kuclín, near Bílina Late Eocene 34-37 Czech Rep. 1/1 Rovno amber Late Eocene 34-37 Ukraine 19/26 Brunstatt, Haut-Rhin Early Oligocene 30-34 France 4/4 Kleinkems Early Oligocene 29-34 Germany 8/10 Auxillac, Auvergne Early Oligocene 28-34 France 1/1 Aix en Provence Middle Oligocene 28 France 7/7 Bitterfeld amber Late Oligocene 23 Germany 23/39 Rott, Westphalia Late Oligocene 23 Germany 3/5 Decín Early Miocene 16-23 Czech Rep. 1/1 Sicilian amber Early Miocene 16-23 Sicily 10/13 Radoboj Early Miocene 19 Croatia 7/15 Mokrina Early Miocene 16-18 Czech Rep. 3/3 Vishnevaya Balka Middle Miocene 11 Southern Russia 1/4 Brünn-Vösendorf Late Miocene 7.5-9 Austria 2/2 Montagne d'Andance Late Miocene 7.5 France 2/2 Joursac, Auvergne Late Miocene 5-7 France 3/3 Caucasus region Late Miocene 5.5-11 Southern Russia 1/2 Schossnitz, Silesia Late Miocene 5-11 Poland 3/3 Oeningen Late Miocene 5.3 Switzerland 6/8 Crete Miocene 5.3-7.2 Greece 1/1 Kerch, Crimea Peninsula Miocene ? Ukraine 1/1 Lac Chambon, Auvergne Pliocene 1.8-5.3 France 2/2

East Palaearctic bioregion Shanwang Early Miocene 17 Shandong (China) 11/18 Chon-Tyz mine Middle Miocene 12-16 Kyrgyzstan 3/3 Chojaburu Middle Miocene 11.6-16 Kyushu (Japan) 1/1

Indomalayan bioregion Borneo amber Miocene Borneo 1/1

Caribbean bioregion Dominican amber Early Miocene 16-19 31/33

Nearctic bioregion Arkansas amber Middle Eocene 40-48 Arkansas 1/3 Green River formation Middle Eocene 40-48 Colorado / 3/12 Wyoming Mossy Creek, near Late Eocene 34-37 Texas 1/1 Wellborn Florissant Late Eocene 34 Colorado 11/19 Quesnel Early Miocene? 20-23 British Columbia 3/4 Mexican amber Middle Miocene 13-20 Chiapas 11/11 Central Alaska Late Miocene 6.7 Alaska 4/4

Afrotropical bioregion Mfwangano Island, Lake Early Miocene 16-23 Kenya 1/1 Victoria Table S2. Number of sites sampled for ants in each habitat type within each bioregion.

Abbreviations for the bioregions studied are as follow: Afrotropical (Afr), Australasian (Aus),

East Palaearctic (Ea Pa), Malagasy (Mal), Nearctic (Nea), Neotropical (Neo), Oceania (Oce),

Indomalayan (In-Ma), West Palaearctic (We Pa). Primary forest (=Pr. Forest).

Afr Aus Ea Pa Mal Nea Neo Oce In-Ma We Pa Desert 13 1 8 0 8 1 0 0 45 Grassland 15 47 40 1 75 26 4 9 210 Pr. forest 32 97 93 27 112 324 11 129 57 Shrubland 61 66 6 0 49 39 2 5 30 Total 121 211 147 28 244 390 17 143 342 Table S3. Ecological classification of ant genera and castes from which fossil specimens have been recovered. The following abbreviations have been used to present the castes: W= workers, G= gyne, M= Male, U= caste unknown.

Genus name Habitat Strata Caste collected Acanthognathus Hypogaeic W Acanthostichus Hypogaeic W Acropyga Hypogaeic G + M Anochetus ALL G Anonychomyrma Epigaeic + Arboreal W + G + M Aphaenogaster Epigaeic W Apterostigma Epigaeic + Arboreal W Azteca Arboreal W + G + M Brachymyrmex Epigaeic + Arboreal U Camponotus Epigaeic + Arboreal W + G + M Carebara Hypogaeic W + G + M Cataulacus Arboreal W + M Cephalotes Arboreal W Cerapachys Hypogaeic U Crematogaster Epigaeic + Arboreal G + M Cylindromyrmex Arboreal G Cyphomyrmex Epigaeic W + G Discothyrea Hypogaeic W + G + M Dolichoderus Arboreal W + G + M Dorymyrmex Epigaeic U Eurhopalothrix Hypogaeic U Forelius Epigaeic U Formica Epigaeic W + G + M Gesomyrmex Arboreal W + G + M Gnamptogenys ALL W + G + M Gracilidris Epigaeic W Hypoponera Hypogaeic G + M Iridomyrmex Epigaeic + Arboreal M Lasius Epigaeic W + G + M Leptogenys Epigaeic + Hypogaeic G Leptomyrmex Epigaeic + Arboreal W Linepithema Epigaeic + Arboreal U Liometopum Epigaeic W + G + M Meranoplus Epigaeic U Messor Epigaeic G Monomorium Epigaeic W Mycocepurus Epigaeic U Myopopone Hypogaeic G Myrmelachista Arboreal U Myrmica Epigaeic W + G + M Neivamyrmex Hypogaeic W Nesomyrmex Arboreal W Nylanderia Epigaeic + Arboreal W + G + M Octostruma Hypogaeic U Odontomachus Epigaeic + Arboreal W Oecophylla Arboreal W + G + M Paraponera Epigaeic + Arboreal W Pheidole ALL W Plagiolepis Epigaeic + Arboreal W + G + M Platythyrea Arboreal W + G Podomyrma Arboreal W Pogonomyrmex Epigaeic W Polyrhachis Epigaeic + Arboreal W Ponera Hypogaeic G + M Prenolepis Epigaeic + Arboreal G Prionopelta Hypogaeic U Pristomyrmex Epigaeic W Proceratium Hypogaeic W + G + M Pseudolasius Epigaeic W Pseudomyrmex Arboreal W + G + M Rhytidoponera Epigaeic W Solenopsis ALL W + G + M Stenamma Hypogaeic M Stigmatomma Hypogaeic W + M Strumigenys Hypogaeic W + G Tapinoma Epigaeic + Arboreal W + M Technomyrmex Arboreal W Temnothorax Epigaeic + Arboreal W + M Tetramorium Epigaeic + Arboreal U Tetraponera Arboreal W + G + M Trachymyrmex Epigaeic W Vollenhovia Epigaeic + Arboreal W Wasmannia Epigaeic + Arboreal U Zatania Epigaeic + Arboreal W + M West Palaearctic East Palaearctic Indomalayan Australasian Afrotropical Malagasy Caribbean Nearctic Neotropical

Figure S1. Map of the bioregions used in this study. Divisions of the world into multiple administrative and geographic regions follow the classification of Guénard et al. 2012.

Reference

Guénard, B., Weiser, M.D. & Dunn, R.R. (2012) Global models of ant diversity suggest regions where new discoveries are most likely are under disproportionate deforestation threat.

Proceedings of the National Academy of Sciences USA, 109, 7368–7373.

Figure S2. Summary of the known distribution for all genera of ants known from fossil deposits and with current distribution. Each row for a given genus indicates its presence for a given bioregion. If coloured then presence known for the specific period, otherwise if blank then presence unknown. Abbreviations are as follow for the geological periods: E= Early, M=

Middle and L= Late. Bioregions are classified according to figure S1. Journal of Biogeography

SUPPORTING INFORMATION

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

ant macroecological patterns

Benoit Guénard, Vincent Perrichot and Evan P. Economo

Appendix S1: Supplementary methods

Assembly of the fossil and modern biodiversity databases

Our dataset of fossil specimens was based on the list established by one of the authors for AntWeb (Perrichot 2014). This list was assembled through a literature search for generic mentions (Brown 1973, Wilson 1985, Lattke 1990, Baroni Urbani & De Andrade 1994, 2003, de Andrade 1994, 1995, 1998, Baroni Urbani, 1995, Poinar et al. 1999, 2006, Baroni Urbani

& De Andrade 2003, Dlussky & Rasnitsyn 2009, Perkovsky 2009, Heterick & Shattuck 2011,

Blaimer 2012, Durán-Ruiz et al. 2013, Wappler et al. 2013, Antropov et al. 2014, Dlussky &

Putyatina 2014), and also complemented by unpublished records from the personal observations by V.P. during his work on institutional and private collections. No deposit older than the early Eocene is known to have fossils of modern ant genera, which limited the number of included deposits. The modern distributions of the genera were extracted from

Guénard et al. (2010, 2012), complemented by the recent relevant taxonomic modifications

(LaPolla et al. 2010, Yoshimura & Fisher 2012), and assigned to specific bioregions.

Definition of the biogeographic regions The Nearctic bioregion is defined here to include all the regions north of Mexico and inclusive of Mexico. Mexico is included to this bioregion on the basis of palaeogeological results suggesting a direct connection between North America and Mexico from the

Paleocene to the Miocene, but not to South America, as the Panama isthmus was not formed yet (Keigwin 1978). However, to fully consider the hypothesis of a more distinct ant fauna

(genera) associated with Mexico and not with the rest of the Nearctic bioregion, we tested the placement of southern Mexico (all the states located south or east of Oaxaca and Veracruz states, with these later two included) within the Neotropical bioregion. As a result, only one genus (Cylindromyrmex, known only from the Caribbean fossil fauna) was excluded from the current Nearctic bioregion. Finally, these alternative classifications of the bioregions did not modify substantially the final results or our conclusions.

Taxonomic classification

Our taxonomic classification followed Bolton (2013), and we took a conservative approach by excluding doubtful records. The record of Ectatomma by Emery (1891) from

Sicilian amber was transferred to Gnamptogenys following Brown and Carpenter (1978). The genera Mycetosoritis and Stenamma were mentioned by Brown (1973) respectively on the base of “possible “male and “shrunken and distorted” specimens from Chiapas amber.

However, the validity of these identifications was later questioned (Baroni Urbani 1980,

Branstetter 2012) and never validated to our knowledge, thus we excluded them from our analysis. Records of Pachycondyla specimens from Eocene amber and imprints (Dlussky

2002, Dlussky & Rasnitsyn 2009, Aria et al. 2011, Dlussky & Wedmann 2012) were not included in our analysis as their current placement is unresolved in the recent taxonomic changes of the genus (Schmidt & Shattuck 2014). It should be noted that several controversies on the placement or validity of specific fossil species or genera exist; with several deposits receiving incomplete or now outdated treatments (e.g. Fushun deposit, Fujian, China)(LaPolla et al. 2013). The data used for the analyses performed here reflect the current state of ant taxonomy and that future work on both fossil and modern taxa could modify the current framework (e.g. the recent changes within the Dorylinae: Brady et al. 2014, or Myrmicinae subfamilies: Ward et al. 2015).

Community database

The literature database was compiled through extensive searches by B.G. during recent projects on the global distribution of Formicidae. Only publications that provided a list of species collected were used so that we could keep the taxonomy up to date (e.g. the

Amblyoponinae, Ectatominae and Proceratiinae subfamilies were once sunk within the

Ponerinae subfamily).

From the 1060 studies with data for 4376 sites, we excluded sites for which only baiting methods were used, which can result in a bias toward more dominant and generalist species (Bestelmeyer et al. 2000). We selected habitats representative of undisturbed or with limited natural disturbance and from which habitat could be categorised as one of the following category: primary forest, shrubland, grassland, or desert. Finally, we also excluded communities with a species richness lower than ten from the NMDS analysis, as their proportions among subfamilies will be noisy due to sampling effects.

The complete list of references used to build this database is presented below.

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