The Arrow Points North – Endemic Areas and Post- Devensian Assembly of the British Empidoidea Fauna (Insecta: Diptera)

Biological Journal of the Linnean Society, 2017, XX, 1–17. With 8 figures.

The arrow points north – endemic areas and post- Devensian assembly of the British Empidoidea fauna (Insecta: Diptera)

ADRIAN R. PLANT1*, TERJE JONASSEN2, PATRICK GROOTAERT3, HANS MEYER4, MARC POLLET5 and MARTIN DRAKE6

1Department of Natural Sciences, National Museum of Wales, Cathays Park, Cardiff CF10 3NP, UK 2NO-4170 Sjernarøy, Norway 3Department of Entomology, Royal Belgian Institute of Natural Sciences, Rue Vautier 29, B-1000, Brussels, Belgium 4Department of Applied Ecology, Institute for Ecosystem Research, Christian Albrechts University of Kiel, Olshausenstrasse 75, D – 24 118 Kiel, Germany 5Research Group Species Diversity (SPECDIV), Research Institute for Nature and Forest (INBO), Kliniekstraat 25, B-1070 Brussels, Belgium 6Orchid House, Burridge, Axminster, Devon EX13 7DF, UK

Received 4 August 2016; revised 13 September 2016; accepted for publication 31 October 2016

Large-scale patterns of species richness, assemblage composition, β-diversity, and endemism in Britain were studied in the Diptera superfamily Empidoidea. Overall species richness was greatest in the south, but two areas of elevated richness in East Anglia and the Northeast Grampian Mountains corresponded with ‘hotspots’ of elevated endemism. Assemblage similarity decayed and species turnover increased along predominantly north–south geographical gradients and between inland and coastal localities. Dispersal direction probability vectors were anisotropic, suggesting that the assembly of northerly British assemblages may have been influenced by dispersal from the south, and eastern English ones by dispersal from continental Europe. Parsimony analysis of endemism retrieved northern localities in ‘basal’ positions with more southerly and European areas in progressively more distal positions in the trees. We propose that British communities were assembled as follows: (1) Early Phase dispersal northwards of cold- adapted taxa between the Devensian Late Glacial Maximum and ~15 Kyr; (2) Mid-Phase colonization by eurythermic taxa at 15–8 Kyr; and (3) Assembly was largely completed by severance of the land bridge with Europe at 8 Kyr with a Late Phase (8 Kyr – present) involving continued northwards dispersal within Britain and partitioning of taxa into geographically restricted habitat refugia.

ADDITIONAL KEYWORDS: community structure – dispersal – diversity – Empidoidea – parsimony analysis of endemism – refugia.

INTRODUCTION considered. Certain geographical regions support many endemic taxa, and understanding such cen- A fundamental problem in ecology and biogeogra- tres of endemicity or endemism ‘hotspots’ at vari- phy is to identify large-scale patterns in diversity ous spatial scales is fundamental to explanations of and assemblage composition of regional biotas and Earth history based on biological patterns (Linder, to understand their historical origins and the pro- 2001). Delimiting areas of endemism is essential cesses by which they are sustained. Endemism is not only in historical biogeography, but also in rec- the extent to which taxa are unique to a particu- ognizing areas of conservation importance (Kerr lar area and is hence dependent on the area scale & Burky, 2002), especially as range restriction is an important component of extinction risk (Purvis *Corresponding author. E-mail: [email protected] et al., 2000; Harvey, 2002).

The mechanisms shaping regional diversity include immature stages present mostly in soils and a wide fine-scale biotic processes – such as speciation, extinc- range of decaying organic material and adults of many tion, dispersal, and species interactions – and broad- are predators of other arthropods and/or nectar feed- scale geographic/geological processes including plate ers. Their near ubiquity and diversity of ecologies and tectonics, changes in sea level or climate, and the for- life-history traits suggests wider utility in studies of mation of topographical barriers to dispersal (Hedges patterns of diversity in Diptera as a whole. et al., 1996). Broad-scale processes influencing the In this study, we investigate the distribution of end- assembly of British biota have been intensively stud- emism, assemblage structure, and species turnover of ied over recent decades. During the last (Devensian) Empidoidea along geographical gradients in Britain. glaciation, probably only southernmost Britain Spatial correlations with area clades retrieved by par- remained ice free (McCabe & Clark, 1998; Clark et al., simony analysis of endemism (PAE) and probabilities 2012), and there is general consensus that the major of dispersal between adjacent areas in Britain and animal and plant colonizations occurred subsequently, near continental Europe then allow historical coloni- driven by glacial retreat and climatic amelioration zation routes to be hypothesized that are reconcilable (Dennis, 1977, 1993; Lowe & Walker, 1984; Roberts, with the post-Devensian geographical and ecological 1989; Coles, 1998; Montgomery et al., 2014) with pole- history of north-western Europe. wards extension of species’ distributions continuing to this day (Parmesan & Yohe, 2003; Mason et al., 2015). Postglacial colonization of Britain has also been docu- MATERIALS AND METHODS mented for insects, especially Coleoptera (Coope, 1975, 1977; Atkinson, Briffa & Coope, 1987) and to a lesser Included taxa extent Diptera, which have been widely used as palae- A total of 827 species of Diptera Empidoidea were oclimatic indicators to characterize historical assem- sampled (Table S1) comprising Dolichopodidae 376, blages in archaeological and sedimentary deposits Empididae 235, Hybotidae 209, Brachystomatidae 3, (Skidmore, 1996; Panagiotakopulu, 2004). The persis- and Atelestidae 2 species. The genera Iteaphila Zett. and tence of relict populations of insects in range-restricted Anthepiscopus Becker each here represented by single areas of Britain but which occur elsewhere in similar species, have not been confidently assigned to any fam- ecological or climatic conditions has often been used ily, and are regarded as incertae sedis in Empidoidea. to infer colonization history of taxa. For example, spe- Data on 678 species were available from Gt Britain cies of many orders of insects with contemporary dis- – Dolichopodidae 291, Empididae 206, Hybotidae 176, tributions restricted to northern British mountains Brachystomatidae 3, and Atelestidae 2 – and on 678 (Horsfield & MacGowan, 1997; Falk & Chandler, 2005; species from continental Europe (Belgium, Germany, Hill et al., 2010; Ball et al., 2011) but which occur else- and Norway) – Dolichopodidae 327, Empididae 173, where in Europe at high latitude or high elevation Hybotidae 173, Brachystomatidae 2, Atelestidae 1, have been considered boreal, boreo-alpine, or boreo- Iteaphila 1, and Anthepiscopus 1. A total of 149 taxa montane relicts. Historically changing climate and were present in continental Europe but not in Britain availability of habitat have resulted in contraction of and the 149 were recorded only in Gt Britain. ranges with the taxa becoming ‘marooned’ in isolated areas of suitable habitat. The Diptera superfamily Empidoidea comprises Sampling methodology the families Empididae, Hybotidae, Dolichopodidae, Data on occurrence of Empidoidea in Great Britain Atelestidae, and Brachystomatidae. They are highly (excluding the Orkney, Shetland, and Scilly islands speciose in Britain with c. 700 species, representing but including the Hebrides, Isle of Man, Anglesey, and c. 10% of British Diptera diversity (based on data in Isle of Wight; hereafter referred to as ‘Britain’) were Chandler, 1998) and can be abundant and a conspicu- collated from a database held by the UK Empid and ous element of the Diptera fauna. Although formal dis- Dolichopodid Recording Scheme (Stubbs, 2010) com- tribution atlases are not available, inspection of 138 prising 138 394 unique taxon/locality/date records 394 unique records collated by the British Empididae of the 678 species. Although all data from 1850 to & Dolichopodidae Recording Scheme (Stubbs, 2010) 2015 were included, 95.07% of records were rela- used in this study indicates multiple types of range tively recent and collected between 1975 and 2015. distributions occur including cosmopolitan species and Data from Belgium, Germany, and Norway were col- those with regional and local range restrictions and lated from databases held by the authors from records eurytopic or stenotopic habitat preferences in terres- made mostly between 1975 and 2015. The raw data trial, aquatic, and littoral environments (Plant, 2003, from both Britain and continental Europe register the 2004; Pollet, 2009). With the exception of the dolichopo- occurrence of taxa in grid squares at variable spatial did Thrypticus Gerstäcker, all species have predatory scales between 10 × 10 m and 10 × 10 km. Analysis of

© 2017 The Linnean Society of London, Biological Journal of the Linnean Society, 2017, XX, 2–17 POST-DEVENSIAN ASSEMBLY 3 local endemism requires careful choice of spatial scale, the north-west quadrant of that square (see Fig. 1). the operational geographical unit (OGU), in order Belgian OGUs were aligned with the UTM grid and to limit geographical recording biases, to minimize were designated as follows: B1, Coastal Western overlap across the boundaries of neighbouring local Flanders (bounded at NW by UTM grid DS77, at SE biomes or across restricted range boundaries, and to by ES13); B2, Inland Western Flanders (ES37, ES73); ensure that data are sufficiently dense to support the B3, Central Flanders (ES93, FR39); and B4, Eastern grid size (Laffan & Crisp, 2003; Plant, 2014a, Mason Flanders (FS58, FS94). Norwegian and German OGUs et al., 2015). Meaningful analysis is unlikely at a scale were referenced by latitude and longitude coordinates, of, for example, 10 × 10 km, at which species rich- not necessarily aligned with the UTM grid. The sin- ness of British Empidoidea varied from 1 to 223 with gle Norwegian grid (designated N1) at the head of a mean of just 29.1, a very low figure compared with Oslofjord was bounded approximately by 59.924°N, the approximately 700 species known from Britain, 9.985°E (NW corner) and 59.480°N, 10.811°E (SE even assuming high levels of patchiness and range- corner). The three German grids were all situated in restriction. The present study routinely analysed the Schleswig-Holstein. They were designated (approxi- occurrence of Empidoidea using grids of 50 × 50 km mate coordinates of NW and SE extremities indicated as OGU (1–413 species, mean 152.3), but in certain in parenthesis) as follows: G1, Sönke-Nissen-Koog cases where density of data was insufficient to sup- NW of Bredstedt, Groß-Jörl NW of Schleswig, port analysis (detailed in Results section), neighbour- Flensburg (54.949°N, 8.697°E; 54.509°N, 9.379°E); ing grids were pooled together into larger area OGUs. G2, Kiel, Flintbek, Preetz, Lütjenburg, Howachter- Each British 50 × 50 km OGU was aligned with the Bucht, Neumünster, Bornhöveder-Seenkette N British Ordnance Survey (OS) grid reference sys- Bornhöved, Plön, Eutin, Bad-Segeberg (54.379°N, tem and was assigned a two-letter prefix code refer- 10.013°E; 53.921°N, 10.715°E); and G3, Grüne Insel ring to the 100 × 100 km OS map reference square Eider Estuary SW of Tönning, Alte Sorgeschleife S in which it occurs and numbered 1–4 clockwise from Bergenhusen, Meldorfer-Bucht W Meldorf (54.396°N,

Figure 1. Location of 50 × 50 km OGUs. Each British OGU was assigned a two-letter prefix code referring to the 100 × 100 km OS map square in which it occurs and is numbered 1–4 clockwise from the north-west quadrant of that square. The single Norwegian grid was designated N1, German grids G1–G3, and Belgian grids B1–B4.

8.701°E; 53.947°N, 9.445°E). The location of all grids do not inform the result, behaving as do autapomor- is shown in Fig. 1. phies in cladistics analysis). An outgroup with an A matrix was constructed recording only presence or all-0 score (all species absent) was arbitrarily estab- absence of taxa, ignoring multiple occurrences at dif- lished, but can be rationalized as the entire history ferent locations or dates within any particular OGU, of Empidoidea assemblages in Britain probably dates resulting in a total of 19 888 (Britain), 1373 (Belgium), from after the last glacial maximum when the country 623 (Germany), and 349 (Norway) unique occurrences was largely ice-covered and most species were likely in 50 × 50 km OGUs. absent. Although it would have been desirable to ana- lyse patterns of local endemism at as high resolution as possible, initial trials using single 50 × 50 km grids General statistical treatment as OGU resulted in highly polytomic tree topologies and graphic presentation and poor bootstrap support for branches, probably Univariate statistics, cluster analysis, and nonmetric because data were insufficiently dense and suffered multidimensional scaling (MDS) were performed in from increased ‘noise’ from poorly recorded, relatively PAST version 3.0 (Hammer, Harper & Ryan, 2001). species-deficient grids. The problem of relative paucity Contour maps of diversity and endemism parameters and patchiness of data at smaller spatial scales was in Britain were prepared by spatial interpolation using overcome by combining, where possible, four geograph- the multiquadric gridding algorithm in the gridding ically adjacent 50 × 50 km grids together as OGUs for module of PAST and the results were superimposed PAE. This ensured that areas analysed (indicated in on outline map outputs from Mapmate Version 2.4.0 Fig. 8) were large enough to provide increased data (MapMate, 2016) and DMAP Version 7.2f (Morton, density and small enough to not markedly overlap the 2016) using image editing software. boundaries of zones of species richness (Fig. 3A), reciprocal weighted endemism (Fig. 3C), and assemblage similarity (Fig. 5) demonstrated elsewhere. Reciprocal weighted endemism Reciprocal weighted endemism was calculated using a modification (Plant, 2014a; Ivković & Plant, 2015) of Coefficient of dispersal direction the method of Moir, Brennen, and Harvey (2009). The The coefficient of species dispersal direction (DD1) was number of OGUs within which each species occurred used as a measure of the probability of species dis- was counted. Each species was then assigned a value persal between different geographic areas (Legendre based on this number, with species known from only & Legendre, 1984). If we identify two separate geo- one OGU being given the highest value of 1, species graphic areas x1 and x2 in which a is the number of spe- occurring in two OGUs given a value of 0.5, species cies in common, b is the number of species restricted to occurring in three OGUs given value of 0.333, and so x1, and c is the number of species restricted to x2, then forth. Total reciprocal weighted endemism for each DD1 can be estimated by: OGU was then calculated as the sum of values for all species whose range overlapped that OGU. Mean a (bc− ) reciprocal weighted endemism was calculated as the DD1()xx12−> = ()ab++c ()ab++c total weighted endemism for each OGU divided by the species richness of that OGU. The term a/(a+b+c) is the Jaccard coefficient of similarity. High values of DD1 result when a is high and Parsimony analysis of endemism b > c supporting the hypothesis of dispersal from x1

Parsimony analysis of endemism (Rosen, 1988) was to x2. When c > b, the value of DD1 has negative sign, performed in TNT Version 1.1 (Goloboff, Farris & supporting the hypothesis of dispersal from x2 to x1 Nixon, 2008) with sufficient memory being allocated (Legendre & Legendre, 1998; Carrara & Flores, 2015). to hold 10 000 trees and general RAM set to 2000 Mb. The geographical areas selected for dispersal studies Traditional parsimony-based searches employed 100 were congruent with areas of assemblage similar- random-addition replicates using tree bisection recon- ity resolved by MDS (Fig. 5) and, where applicable, nection (TBR) branch swapping, retaining 10 trees included hotspots of reciprocal weighted endemism per replication with ‘characters’ uniformly weighted (Fig. 3C). The included areas are indicated in Fig. 7 and (prior-weighted) and unordered. Bootstrap support designated as follows: East Anglia (zone A; comprising was calculated using 1000, replicates, and consist- the following 50 × 50 km OGUs: TF3, TG3, TG4, TL2, ency index (CI) and retention index (RI) were deter- TM1, TM2); south-east England (zone B; SU1, SU2, mined by running the stats.run script. Taxa present in SU3, SU4, TQ1, TQ2, TQ3, TQ4, TR1, TR4, SZ1, SZ2, only one OGU were removed from the analysis (they TV2); south-west England (zone C; SS2, SS3, SS4 ST1,

ST4, SX1, SW2, SX3, SY1); Wales (zone D; SH1, SH2, SH3, SH4, SN1, SN2, SN3, SM4, SM3); north-east England (zone E; NZ3, SE2, SE3, TA1, TA4, TF1, TF2); northern England (zone F; NY3, SD2, NZ4, SE1, SE4, SJ2, SK1); highlands of Scotland (zone G; NH1, NH2, NH3, NH4, NJ1, NJ2, NJ3, NJ4, NK1, NK2, NN1, NN2, NN3, NN4, NO1, NO2, NO3, NO4); and north- west highlands (zone H; NB1, NB2, NB3, NB4, NC1, NC2, NC3, NC4, ND1, ND4, NF2, NF3, NG1, NG2, NG3, NG4, NM1, NM2, NM3, NM4).

B-Diversity Species turnover (β-diversity) was calculated using

Whittaker’s measure βw (Whittaker, 1960) in PAST; βw = (S/α) − 1, where S = the total number of species recorded and α = the mean sample diversity where each sample is a standard size (1 OGU) and diversity is measured as species richness. Values of βw range between 0 (complete identity) and 1 (complete non-identity).

RESULTS

Patterns of diversity in britain Species richness Near complete sampling of British Empidoidea species was achieved from 138 394 unique taxon/locality/ date records of the 678 species representing ~98.6% of Figure 2. Geographical distribution of recorded sites in Gt. all known British empidoid Diptera species. Sampling Britain. Localities where at least one species of Empidoidea effort covered the entire country but was uneven with is recorded are plotted as a resolution of 5 × 5 km. greater coverage from areas of southern and north-east England, parts of Wales and the Cairngorm Mountains, Strien, van Swaay & Termaat, 2013; Isaac et al., 2014), and Strathspey areas of Scotland for example, with they were not applied here. However, ‘cold-spots’ of regions of central England and many areas in Scotland species richness are almost certainly not due entirely which are less well covered (Fig. 2). Geographical bias to inadequate recording effort as ecological and habi- is an inevitable consequence of data collected by bio- tat considerations lead us to expect that areas such as logical recording schemes (Isaac & Pocock, 2015) as the uplands in the north or zones of extensive arable records are collected by volunteers of variable experi- agriculture in the eastern English Midlands would ence at times and places that suit them and tend to have a depauperate fauna compared with, for example, group around localities where volunteers live or places ancient woodlands or landscapes with heterogeneous they target as being diverse or interesting in some habitat elements found elsewhere. other way. Recorder effort is thus neither systematic nor randomized and presents considerable problems of analysis. When species richness (number of species) Endemic areas was mapped at the scale of 50 × 50 km OGUs (Fig. 3A) Figure 3B shows how total reciprocal weighted end- and compared with geographical coverage (Fig. 2), emism of Empidoidea varied across Gt Britain. High some degree of correlation is observed although cer- endemism was apparent in southern and north-east tain areas such as N Wales and NW England have England, south-east Wales, and especially East Anglia fewer species than might be expected from the high (hereafter abbreviated to EAng, delimited here by level of coverage there. Failure to record a species does grids TG, TM, and eastern TF and TL in Fig. 1) and not of course preclude its presence, and although sta- the Northeast Grampian Mountains of the Scottish tistical occupancy models have been developed that Highlands (hereafter abbreviated as NEGM, compris- can potentially ‘plug’ gaps in coverage (Hill, 2012; van ing grids NJ, NO, NN, and eastern NH in Fig. 1). Low

Figure 3. Geographical distribution of species richness and endemicity of Empidoidea in Gt. Britain. (A), species richness (number of species present); (B), total reciprocal weighted endemism; (C), deviation of mean reciprocal weighted endemism from values predicted by a regression model of its relationship with species richness. Spatial interpolation of results for 50 × 50 km OGUs was performed in PAST using the multiquadric gridding algorithm.

Figure 4. Relationship between mean reciprocal weighted endemism and species richness in 50 × 50 km OGUs in Gt. Britain. Mean values ± standard error are indicated. Linear regression (r = 0.581) was fitted (dashed line) using the model- ling module in PAST and 95% confidence intervals (unbroken lines) determined from 2000 bootstrap replicates. Strongly positive ‘outlier’ OGUs are indicated (see Fig. 1 for explanation of alphanumeric code). endemism was found in areas bordering the western possible that detection of a larger number of endemic seaboard, English Midlands, Scottish Lowlands, and species might be a consequence of increased coverage. the far-north of Scotland. Areas of high endemism Mean reciprocal weighted endemism and species rich- were similarly distributed to those with high species ness were indeed weakly correlated (Fig. 4), and it is richness (Fig. 3A), suggesting that high species rich- interesting to note that positive ‘outlier’ OGUs with ness correlates with high endemism. Alternatively, as mean weighted endemism above that predicted by the areas of high endemism were also generally coincident regression line in Fig. 4 were distributed across the with those with better observer coverage (Fig. 2), it is full range of variation in species richness and likely

© 2017 The Linnean Society of London, Biological Journal of the Linnean Society, 2017, XX, 6–17 POST-DEVENSIAN ASSEMBLY 7 represent OGUs with exceptionally high endemism. ≥125 species). The result was transformed into a more While coverage effects cannot be entirely excluded, readily interpretable form by subjecting the data from a better representation of the geographical spread the primary axis of the MDS result to cluster analy- of endemism was obtained by mapping deviations in sis using Euclidian distance (Fig. 5). Although assem- mean weighted endemism above and below the regres- blages represented by adjacent clusters were generally sion line in Fig. 4. The resulting map (Fig. 3C) thus associated with adjacent geographical areas, those of shows areas with relative levels of endemism that devi- Scotland (cluster 1 in Fig. 5) were distinctly different ate above or below which expected from their species from those elsewhere in Britain, indicating that the richness (and concomitantly, coverage). In this treat- species composition of assemblages differed greatly in ment, the endemic areas of EAng and NEGM are again the two areas. A group of East Anglian OGUs (clus- retrieved and a new endemic area in the far north of ter 2) had a sister-group relationship with other areas Scotland (grid NC in Fig. 1) is weakly apparent, but of England within which two clusters were retrieved: the southern and north-east English and south-east cluster 3 representing south-east England and clus- Wales ‘hotspots’ are greatly diminished in apparent ter 4 including south-west and northern England and importance. Wales. Overall, the results indicate zones of Empidoidea assemblage similarity orientated approximately along a south-east to north-west axis across Britain but with Assemblage composition and species turnover those associated with the Scottish Highlands and East In order to examine similarities in Empidoidea assem- Anglian endemic areas being more distinctly defined. blages present in endemic areas and elsewhere, we Variation in species turnover along geographical employed MDS using Jaccard index to compare only gradients was further investigated using Whittaker’s relatively data-rich 50 X 50 km OGUs (those with measure of β-diversity, βw (Fig. 6). TG4 is an OGU at

Figure 5. Assemblage similarities of British Empidoidea. (A), a two-dimension MDS matrix was calculated using Jaccard similarity in PAST (stress = 0.1608) utilizing only 50 × 50 km OGUs that have at least 125 species present. Data from the first axis of the MDS result were then analysed using unweighted pair-group average cluster analysis in PAST employing Euclidian distance. Numbers 1–5 indicate major clusters discussed in the text. (B), map of OGUs colour-coded to match major clusters in A.

Figure 6. β-Diversity of British Empidoidea. Pairwise comparisons of Whittaker’s measure of β-diversity (βw) were made between TG4 (A), NH3 (B), and SU4 (C) and all other 50 × 50 km OGUs in which Empidoidea were recorded. Values of βw range between 0 (complete identity) and 1 (complete non-identity). Spatial interpolation of results was performed in PAST using the multiquadric gridding algorithm. the centre of the EAng endemism hotspot, and pair- Germany, but vectors for other trans-North Sea coloni- wise comparison of βw between it with all other British zation possibilities (e.g. between Belgium and south- OGUs revealed pronounced east-west and south-east– east England (zone B) or north-east England (zone E) north-west gradients of dissimilarity (Fig. 6A). As spe- and Germany) were weak. The finding of a prevalent cies turnover measured as βw provides an accurate anisotropic directional dispersal vector in Britain reflection of community turnover (Wilson & Shmida, is consistent with the historical foundation of more 1984), it is clear that assemblage similarity decays northerly assemblages of Empidoidea by dispersal in with distance along these axes. The gradient of turno- a northerly or north-westerly direction from ‘founder’ ver at distance from NH3 in the NEGM hotspot was assemblages further south. Assemblages in eastern less pronounced (Fig. 6B) but with some similarity England may have been influenced, at least in part, in assemblage composition likely being maintained by colonization from regions that now form adjacent through inland localities further south, while coastal areas of the modern continental European landmass areas in both the east and west were clearly very dif- and those of northern Germany in Schleswig-Holstein ferent. Turnover away from SU4 in central southern have been shaped by dispersal from the south. England had a strong north–south component and again, large differences were evident from coastal Parsimony analysis of endemism localities. PAE employing 650 taxa and 28 ingroup OGUs constructed by combining four geographically adjacent 50 × 50 km grids in Britain and one OGU comprising four Community history 50 × 50 km grids in Belgium retrieved two equally par- Dispersal direction simonious trees (CI = 0.236, RI = 0.519). Resampling Figure 7 summarizes measurement of the coefficient support (Fig. 8A) was generally low, although a ter- of dispersal direction, DD1, between regions of Britain minal area clade incorporating all southern localities and continental Europe. DD1 can be thought of as a (indicated by branches distal to the arrow in Fig. 8A) measure of the probability that species in an assem- was very robust being supported by all bootstrap rep- blage in one area are derived from another (Legendre licates. More northerly British OGUs were retrieved & Legendre, 1984). Values of DD1 were strongly in ‘basal’ positions in the tree topology, whereas south- asymmetric across different regions of Britain, indi- ern and eastern English and the Belgian OGUs were cating a common dispersal direction vector trending resolved in more terminal positions. German and from southern areas toward the north or north-west. Norwegian data were not included in the analysis Strong dispersal vectors were also found directed from above (Fig. 8A) because PAE ideally requires OGUs to Belgium to East Anglia (EAng) (zone A in Fig. 7) and to have identical areas (Laffan & Crisp, 2003). It should

Figure 7. Coefficients of dispersal direction of Empidoidea assemblages between regions of Britain and continental Europe. Values of the coefficient of dispersal direction (DD1) are indicated. The direction of dispersal vectors between regions (indicated by DD1 with positive sign) is shown by the arrows with thickness approximately proportional to the value of DD1. Regions are indicated by, (A), East Anglia; (B), south-east England; (C), south-west England; (D), Wales; (E), north-east England; (F), northern England; (G), highlands of Scotland, and (H), north-west highlands. be noted, however, that geographical land area was not topology implying a north–south gradient with older constant in British OGUs as all coastal OGUs inevita- ancestry in the north and younger in the south. bly had actual land areas reduced by the presence of sea. When the German (three 50 × 50 km grids) and Norwegian (one 50 × 50 km grid) data were grouped DISCUSSION and included as OGUs, PAE (678 included taxa, 30 ingroup OGUs) retrieved 2 equally parsimonious trees This study has revealed that geographical areas of (CI = 0.219, RI = 0.494), and the bootstrap consensus Britain with high species richness of Empidoidea gen- (Fig. 8C) had similar topology and branch support to erally correspond with the areas of range-restriction as that obtained when German and Norwegian data were measured by reciprocal weighted endemism (Fig. 3B). excluded. The German and Norwegian localities were An association between high levels of endemism and retrieved in a terminal area clade that also included species richness is perhaps not unexpected as it is rea- southern localities. The results suggest that the his- sonable to suppose that rarer range-restricted species torical assembly of communities now represented by are more likely to persist in ecologically ‘intact’ and modern assemblages in the north of Britain may have varied areas that provide greater ecological oppor- preceded the assembly of those further south with tree tunity and are able to support a greater number of

© 2017 The Linnean Society of London, Biological Journal of the Linnean Society, 2017, XX, 9–17 10 A. R. PLANT ET AL. species. Indeed, correlations between hotspots of local those identified by Plant (2014b) employing a much endemism (measured as rarity) and elevated species smaller number of species (205) of just one empidoid richness have also been reported in Britain for other family (Empididae). Tables 1 and 2 list Empidoidea taxa, for example birds (Gibbons et al., 1996), and else- taxa considered as narrow range endemics in a British where for Diptera (Ivković & Plant, 2015). The topo- context and characteristic of the EAng and NEGM hot- graphical delimitation of areas of local endemism was spots, respectively. Species with core ranges centred robust and endured when geographical bias in record- within these two areas but demonstrating distinct ing effort was moderated by considering only devia- geographic range disjunctions or with ranges partially tions above the expected relationship between mean overlapping adjacent areas are also indicated. Species reciprocal weighted endemism and species richness composition of Scottish Empidoidea assemblages as (Fig. 4) as indications of local endemic areas (Fig. 3C). assessed by MDS was markedly dissimilar from that Two principal areas of local endemism were recov- in the rest of Britain (Fig. 5, cluster 1) although NEGM ered, in EAng in eastern England and the NEGM of assemblages were not well resolved from others in the Scottish Highlands, with less significant zones Scotland. The EAng assemblage of Empidoidea (Fig. 5, associated with southern England and the far north of cluster 2) was clearly structured differently from Scotland. The areas identified here are coincident with others in England and Wales, which were otherwise

Figure 8. Parsimony analysis of endemism of British and continental European Empidoidea. (A), bootstrap consensus of two equally parsimonious trees resolved by PAE using 650 taxa, and 28 OGUs comprising four pooled adjacent 50 × 50 km grids in Britain and Belgium, CI = 0.236, RI = 0.519; (B), geographical alphanumeric codes V1–V27 identifying British OGUs used in the analysis; (C), terminal part of bootstrap consensus of two equally parsimonious trees resolved by PAE using 678 taxa, and 30 OGUs comprising four pooled adjacent 50 × 50 km grids in Britain and Belgium, three pooled grids from Germany, and a single grid from Norway, CI = 0.219, RI = 0.494. The basal part of the tree (basal to the arrow in A and C) had identical topology as in A. Bootstrap support (1000 replicates) is indicated at the nodes.

Table 1. Taxa considered characteristic of the East Anglian hotspot of endemism (EAng)

Taxon Family Distribution status

Hilara hirtella Collin Empididae N Rhamphomyia breviventris Frey Empididae N Platypapus pallidiseta Kovalev Hybotidae N Platypalpus pygialis Chvála Hybotidae N Achalcus nigropunctatus Pollet & Brunhes Dolichopodidae N Cyturella albosetosa (Strobl in Czerny & Strobl) Dolichopodidae N Dolichopus kerteszi Lichtwardt Dolichopodidae N Dolichopus laticola Verrall Dolichopodidae N Dolichopus nigripes Fallén Dolichopodidae N Dolichopus plumitarsis Fallén Dolichopodidae N Hercostomus verbekei Pollet Dolichopodidae N Neurigona abdominalis (Fallén) Dolichopodidae N Poecilobothrus majesticus d’Assi Fonseca Dolichopodidae N Empis prodromus Loew Empididae W Platypalpus caroli Grootaert Hybotidae W Achalcus thalhammeri Lichtwart Dolichopodidae W Campsicnemus magius (Loew) Dolichopodidae W Dolichopus migrans Zett. Dolichopodidae W Thrypticus smaragdinus Gerstaecker Dolichopodidae D Achalcus vaillanti Bunhes Dolichopodidae D Telmaturgus tumidulus (Raddatz) Dolichopodidae D

Distribution status; N, narrow-range endemic confined to the EAng hotspot; W, distribution centred on the EAng hotspot but encroaching on adjacent areas; D, disjunct distribution including the EAng hotspot and distant areas. resolved by MDS into two groups (Fig. 5, clusters 3 & PAE retrieved a nested set of area clades with more 4), one occupying much of central England and the northerly British OGUs recovered in ‘basal’ positions other extending from south-west England through and more southerly British and continental European Wales into northern England. Thus, disparate species localities in progressively more distal positions in composition of the EAng and NEGM centres of end- the tree topology (Fig. 8). Branch support was gen- emism is also supported by ordination. erally low although much stronger for the terminal

Species turnover (measured as βw) increased along area clade including all southern localities (indicated spatial gradients away from the EAng (Fig. 6A), NEGM by the arrow in Figs 8A, C), which emulates a corre- (Fig. 6B) and southern English (Fig. 6C) centres of sponding geographical separation between Scottish endemism. Decay of community similarity with dis- assemblages and those of the rest of Britain found by tance is well known as a scale-dependant effect (Keil ordination with MDS. There was general geographi- et al., 2012) generally attributed to environmental and cal correspondence between tree topology and area climatic dissimilarities along geographical gradients clades found by PAE with areas of elevated recipro- (Nekola & White, 1999; Hawkins et al., 2003; Field cal weighted endemism and assemblage similarity. et al., 2009) influencing both niche- and dispersal- We interpret the results as evidence that historical based community assembly mechanisms (Sokol et al., community assembly processes that gave rise to con- 2011). Our data revealed decay in species similarity temporary northern assemblages in Britain preceded of Empidoidea assemblages orientated predominantly those that eventually gave rise to more southerly along south-east to north-west gradients and between communities. Biotic connections shared by south- coastal and inland localities, which are patterns of var- ern assemblages are more recent than those further iation that are widespread in the British biota (Hill, north. Furthermore, a tree topology lacking in deep 1991; Harrison, Ross & Lawton, 1992). Gradients were branches suggests that all modern British assem- not uniform as, for example, upland areas of northern blages are descendants of a single early pioneer com- England and Wales were less dissimilar to the NEGM munity (or at least that if multiple pioneer events area than were adjacent lowland areas (Fig. 6B), indi- occurred, they must have been at an early time in the cating that local-scale environmental conditions are history of Empidoidea being present in Britain). The likely superimposed on the form of wider-scale geo- results imply a north–south gradient between early graphic gradients. ‘founder’ assemblages in the north and southern

Table 2. Taxa considered characteristic of the Northeast Grampian hotspot of endemism (NEGM)

Taxon Family Distribution status

Hilara hybrida Collin Empididae N Hilara submaura Collin Empididae N Platypalpus pygmaeus (Mg.) Hybotidae N Rhamphomyia aethiops Zett. Empididae N Rhamphomyia albidiventris Strobl Empididae N Rhamphomyia hirtula Zett. Empididae N Rhamphomyia ignobilis Zett. Empididae N Rhamphomyia vesiculosa (Fallén) Empididae N Tachypeza truncorum (Fallén) Hybotidae N Wiedemannia phanstasma (Mik) Empididae N Wiedemannia simplex (Loew) Empididae N Medetera infumata Loew Dolichopodidae N Dolichocephala thomasi Wagner Empididae S Bicellaria halterata Collin Hybotidae S Clinocera nivalis (Zett.) Empididae S Hilara abdominalis Zett. Empididae S Platypalpus tuomikoskii Chvála Hybotidae S Rhamphomyia albosegmentata Zett. Empididae S Rhamphomyia trigemina Oldenberg Empididae S Hydrophorus rufibarbis Gerstëcker Dolichopodidae S Dolichopus maculipennis Zett. Dolichopodidae S Platypalpus confinis (Zett.) Hybotidae SD Rhaphium lanceolatum Loew Dolichopodidae SD Heleodromia irwini Wagner Brachystomatidae D Hilara barbipes Frey Empididae D Hilara hirta Strobl Empididae D Hilara diversipes Strobl Empididae D Platypalpus alter (Collin) Hybotidae D Platypalpus ecalceatus (Zett.) Hybotidae D Platypalpus stigmatellus (Zett.) Hybotidae D Rhamphomyia murina Collin Empididae D

Distribution status; N, narrow-range endemic confined to the NEGM; S, distribution centred on the NEGM but encroaching on adjacent areas; D, disjunct distribution including the NEGM and distant areas. assemblages influenced by more recent events. PAE among groups of organisms can be reconciled with has been widely used as a method to generate his- geological evidence or palaeoecological data (Rosen, torical hypotheses of biogeographical area relation- 1988). ships (García-Barros et al., 2002; Navarro et al., Climate changes in Europe during Pleistocene glaci- 2007; Plant, 2014a; Ivković & Plant, 2015). The tech- ation episodes were associated with periodic expansion nique has attracted criticism including a perceived and contraction of northern temperate taxa which sur- inability to distinguish between areas sharing simi- vived in refugia during glacial maxima and extended lar ecologies and those with similar history (Rosen, their ranges during interglacials (Montgomery et al., 1988) and questions as to the relative strength and 2014). During the Devensian Late Glacial Maximum importance of geographical patterns generated by (LGM) 26.5–19 Kyr, much of Britain and Ireland was vicariance and by dispersal (see Nihei, 2006 for dis- covered by ice (McCabe & Clark, 1998; Clark et al., cussion). A major limitation of PAE is that it ignores 2012) with limited exposure of land (Rolfe et al., 2012; phylogenetic relationships (Humphries, 1989, 2000), Clark et al., 2012) and only a very restricted fauna but there can be greater confidence that the results of cold-adapted species is likely to have persisted in reflect historical events if they can be corroborated southern Britain. Following the LGM, a period ensued with the results of traditional cladistic biogeogra- of rapid changes in ice extent, sea levels, and climate phy based on a sound knowledge of phylogeny (una- followed by steady warming from 15 Kyr, punctuated vailable for Empidoidea) or if geographical patterns by the cooler Younger Dryas (12.8–11.5 Kyr). From the

© 2017 The Linnean Society of London, Biological Journal of the Linnean Society, 2017, XX, 12–17 POST-DEVENSIAN ASSEMBLY 13 start of the Holocene (11.5 Kyr), a more stable climate 5000–7000 years characterized by fluctuating but gen- ensued, continuing to the present day (Montgomery erally cool climates when ice-free habitat may have et al., 2014). Land connectivity between eastern been available at different places at different times Britain and Europe via Doggerland persisted until c. (Montgomery et al., 2014). Diptera are a dominant 8Kyr when the land bridge between Britain and the component of many modern high Arctic arthropod Netherlands and Belgium was inundated (Coles, 1998; communities (Danks, Kukal & Ring, 1994; Brodo, 2000) Montgomery et al., 2014). As temperatures rose, less and, for example, many genera of the empidid sub- cold-tolerant species, which had been restricted to family Empidinae, especially Rhamphomyia Mg. are southerly refugia (Stewart et al., 2010), would have speciose and numerous at high latitudes and at high dispersed out of these areas to colonize Britain and elevations where they can be important pollinators north-western Europe, and there is abundant evidence (Lefebvre et al., 2014; Vajda, 2015). Whereas species from the palynological and archaeobiological records, of the empidine genera Rhamphomyia and Hilara Mg. sedimentary fossil deposits, and phylogeographic stud- comprise only c. 17% of the total British Empidoidea, ies, of major colonizations of Britain and Doggerland they constituted 45% of narrow range endemic taxa by plants and animals during this period (Lowe & here considered characteristic of the NEGM end- Walker, 1984; Coles, 1998; Montgomery et al., 2014) emism hotspot (Table 2). While knowledge of global before severing of the land bridge presented a barrier ranges of these species is limited, all appear to have to dispersal. northern European distributions, sometimes with Our PAE results reveal that the historical assembly disjunct populations in central European mountain of Empidoidea communities now represented by mod- ranges, and might properly be considered as boreal or ern assemblages in much of Scotland likely took place boreo-montane taxa. These species (and indeed other at an early stage in the origination of the British fauna. non-empidine taxa listed in Table 2) may be relicts This does not imply, of course, that the composition of of an Early Phase of Diptera colonization of Britain modern northern assemblages actually matches that of by cold-adapted stenotherms dating to the early post- their progenitors, but rather that it was derived from Devensian (between the LGM and 14–15 Kyr) or them. A consistent south to north vector of historical even to the LGM, although a later colonization dur- dispersal direction probabilities (Fig. 7) together with ing cold climatic periods such as the Younger Dryas a similarly orientated decay in assemblage similarity cannot be discounted. The Grampian Mountains, may be linked to Holocene climatic amelioration allow- especially their included areas of Strathspey and the ing northward migration of eurythermic taxa, which Cairngorm Mountains, are well known as loci of range- would, in effect, have diluted the signal of early cold- restricted species of many Diptera families includ- adapted pioneer communities which themselves would ing Heleomyzidae, Calliphoridae, Scatophagidae, have retreated northwards as the climate warmed. Anthomyiidae, Muscidae (Horsfield & MacGowan, Early British and continental European Empidoidea 1997), Mycetophilidae, Phoridae, Pipunculidae (Falk shared a common origin as judged by PAE as Belgian, & Chandler, 2005), Syrphidae (Ball et al., 2011), and German, and Norwegian assemblages were retrieved other orders of insects including Lepidoptera (Hill in terminal nested area clades of the tree (Fig. 8). Our et al., 2010), Odonata (Merritt, Moore & Eversham, data are consistent with a model in which British and 1996), and Neuroptera (Kirby, 1991). Many Grampian continental assemblages were derived from common range-restricted species are confined to montane habi- ancestral communities which probably came to occupy tats such as snowfield vegetation and tundra-like ice-free land in north-western Europe following the habitats (Horsfield & MacGowan, 1997; Horsfield, end of the Devensian glaciation and at a time before 2002; Sinclair, 2008) or associated with boreal wood- the land-bridge between Britain and Europe was lost. land remnants of Populus tremula and Pinus sylvestris Northward dispersal of more southerly communities (Horsfield & MacGowan, 1997; MacGowan, 1997) and would have continued into at least the mid-Holocene. may be Early Phase colonists of Britain. The lack of any deep branching in PAE tree topology By 13 Kyr, the severe periglacial conditions of the reveals no evidence consistent with a vicariant sepa- Late Devensian were rapidly ameliorating, and not- ration of the British fauna that might be attributed withstanding the intercession of the cold Younger to the relatively recent (8 Kyr) loss of land connectiv- Dryas, there are indications that summer tempera- ity with Europe, suggesting that the assembly of the tures in much of Britain were little different from the British fauna was largely complete by the time the present day (Lowe & Walker, 1984). Transition from land-bridge was inundated. Arctic conditions may have been abrupt at some sites Empidoidea exhibit very varied ecologies and envi- as judged by biostatigraphic evidence of Coleoptera ronmental tolerances, and some cold-tolerant taxa, assemblages (Coope, 1975, 1977). Although at the at least, were likely to have persisted in southern- start of the Holocene, Britain and Doggerland likely most Britain through the LGM and the following had only sparse woodland cover, perhaps on account of

© 2017 The Linnean Society of London, Biological Journal of the Linnean Society, 2017, XX, 13–17 14 A. R. PLANT ET AL. the immaturity of soils, more extensive forests devel- are the major components of the EAng hotspot oped subsequently (Coles, 1998) and greater ecological (Table 1), and many of the included species have opportunity would have allowed increased coloniza- wetland or coastal affinities. The fen and breckland tion by Diptera, especially Empidoidea, the majority of habitats of EAng are recognized as centres of distri- which have predatory immature stages found in well- bution of many range-restricted taxa including cer- developed soils and decaying organic matter. Ireland tain aquatic Heteroptera (Huxley, 2003) and Odonata has been isolated as an island for perhaps twice as long (Merritt et al., 1996) and species of the Diptera fami- as Britain and there is no evidence that a land bridge lies Syrphidae (Ball et al., 2011) and Mycetophilidae between these islands persisted after 15 Kyr (Edwards (Falk & Chandler, 2005). Such habitats may formerly & Brooks, 2008). Although the Irish fauna was not have been more widespread as some species with a core studied here, it shares only 50.1% of its Empidoidea distribution in EAng have modern ranges that include diversity with modern Britain (based on the data of geographically disjunct outlier populations elsewhere. Chandler, 1998). It thus seems likely that the Middle For example several species of Diptera associated with Phase of colonization of Britain by Empidoidea was Phragmites (often the dominant plant in fen habitats) underway by 15 Kyr and that major colonization of have isolated populations in distant localities with Britain continued after the loss of the Ireland-Wales abundant Phragmites in southern Britain and the land bridge and probably accounts for the assembly of fen and open water species Allodia protenta Laštovka the majority of nonboreal lowland communities now & Matile (Mycetophilidae) and Anopheles algerien- present. The middle phase would have been termi- sis Theobald (Culicidae) are also known from similar nated by the inundation of Doggerland and loss of the habitats in Anglesey in Wales (Falk & Chandler, 2005). land bridge between Britain and continental Europe Interestingly, ordination of species composition of at 8 Kyr, after which the presence of open marine envi- Empidoidea implies similarities between assemblages ronments would have presented barriers to further on Anglesey (Grid SH1) and part of EAng (Fig. 5, dispersal and colonization. The dispersal capabilities cluster 3a), both areas with extensive fen habitat. We of Empidoidea are very poorly known, and we have no suggest that although the EAng hotspot of endemism evidence to indicate to what extent they would have may have originated during mid-phase colonization of been able to penetrate Britain in the Late Phase once Britain, it was probably shaped and became more geo- the land-bridge was lost, and can only speculate that graphically restricted by subsequent habitat changes. colonization rate was likely much slower than during Such changes were likely to have been substantial for the preceding period. fen species, which would have suffered massive loss of While the NEGM endemism hotspot might be habitat through anthropogenic wetland draining dur- understood as a montane refugial area into which cold- ing the late phase. adapted Early Phase colonists retreated northwards Disjunctions are also known between areas of the in the face of climatic amelioration, origination of the Scottish Highlands and English localities. These EAng hotspot is less clear. The close terminal posi- typically involve heathland species such as the tions of East Anglian and Belgian OGUs in PAE trees Syrphidae Microdon analis (Macq.) (Ball et al., 2011) (Fig. 8) suggest a relatively recent common origin, and and may represent examples of populations becom- dispersal direction vectors indicate that the assembly ing ‘marooned’ in isolated pockets of acidic healthy of East Anglian communities may have been consid- soils during historical edaphic or other environmen- erably influenced by Belgian and south-east English tal changes. We have no clear evidence for disjunct faunas (Fig. 7). The alluvium-filled basins and surface distributions among the many heathland specialist sands and gravels of EAng (Greig, 1996) and similar Empidoidea. However, ordination suggested similari- surface topography, at least in the west of Belgium ties in assemblage composition between the Scottish (Verbruggen, Denys & Kiden, 1966), sustain similar Highlands and grid SO1 on the Welsh/English bor- broad habitat types including fen and sandy heath or ders (Fig. 5, cluster 1a). Species characteristic of pseudo-steppe environments which were also likely this disjunction include Hilara barbipes Frey, Hilara present on Doggerland during the Holocene (Coles, diversipes Strobl, Hilara pseudosartrix Strobl, and 1998). The inundation of Doggerland at c. 8 Kyr marked Platypalpus stigmatellus (Zett.); and assemblage sim- the final loss of land connectivity between Britain and ilarity is also supported by a larger number of spe- continental Europe and would have resulted in some cies such as Oedalea ringdahli Chvála, Platypalpus components of the shared Doggerland biota becoming melancholicus (Collin), and Dolichopus argyrotarsis isolated in refugial areas on either side of the North Wahlberg that have essentially northern and western Sea in EAng and Belgium. distributions but with relatively isolated and small Whereas the taxonomic composition of Empidoidea populations not only on the Welsh borders, but also in the NEGM hotspot is dominated by cold-adapted elsewhere in predominantly upland areas of England. Empididae and Hybotidae (Table 2), Dolichopodidae Many of the species involved have associations with

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SUPPORTING INFORMATION Additional Supporting Information may be found in the online version of this article at the publisher’s website: Table S1. List of taxa of Empidoidea included in analyses.