Once upon a time in Mexico: Holocene phylogeography of the spotted bat

21 Holocene-era range expansions are relevant to understanding how a species might respond to the warming 22 and drying climates of today. The harsh conditions of North American deserts have phylogenetically 23 structured desert bat communities but differences in flight capabilities are expected to affect their ability 24 to compete, locate, and use habitat in the face of modern climate change. A highly vagile but data-25 deficient bat species, the spotted bat ( Euderma maculatum ) is thought to have expanded its range from 26 central Mexico to western Canada during the Holocene. With specimens spanning this latitudinal extent, 27 we coupled phylogeography (mtDNA) with ecological niche modeling (ENM) to investigate the 28 Holocene biogeography from the rear to leading edges. The ENM and phylogeny supported a Holocene 29 range expansion from Mexico with increased expansion throughout the intermountain west within the last 30 6 kya. Long-term isolation at the southern-most margin of the range suggests one or more populations 31 were left behind as climate space contracted and are currently of unknown status. The species appears 32 historically suited to track shifts in climate space but differences in flight behaviors between leading edge 33 and core-range lineages suggest that range expansions could be influenced by differences in habitat 34 quality or climate (e.g., drought). Although its vagility could facilitate the tracking of environmental 35 change and thereby extinction avoidance, anthropogenic pressures at the core range could still threaten the ability for beneficial alleles to expand into the leading edge.


Introduction 38
Modern-day climate change is an existing and threatening influence on the distribution of biodiversity

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(1,2). Western North America is becoming warmer and drier (3,4), a trend that is already shifting the ability to compete, locate, and use habitat warming and drying climate of today may vary by their species-61 specific dispersal characteristics (17). In general, species capable of shifting their range with changing 62 climates can avoid extinction (18) and long distance dispersal is expected to play a critical role toward 63 that end (19).

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The spotted bat (Euderma maculatum) exhibits long flight capabilities and large home range sizes 65 relative to many Vesper bats in North America (20), and has a poorly understood biogeographic legacy.

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Its three white, dorsal spots, large ears, and an audible, low-frequency call are charismatic hallmarks for 67 identification (21-23). However, this charismatic bat is rarely observed. The species occupies a patchy, Phylogeography of the spotted bat 4 68 widespread range, and is associated with rugged environments from central Mexico to British Columbia 69 (BC), Canada (22,24,25) (Fig 1). The species largely occupies desert and xeric shrubland biome but 70 individuals at the leading edge occupy an area broadly associated with the temperate coniferous forest 71 biome (26) (Fig 1). The space used by individuals on the leading edge, however, is semi-arid, resembling 72 elements of habitat in the core range (23). In British Columbia, the northern-most extent of its range, E. background that exceeded the constraints of the occurrences to provide more flexibility in generating 162 background points (S1 Fig 1). We trained Maxent models with an 80:20 split of the occurrences for 163 training and testing. We used three sets of randomly sampled background points (n = 120 per set) and ran 164 the model through 10 evaluations. Each set of evaluations for a model were then combined into a full 165 model. We evaluated the models using the area under the receiving operating curve score for training and

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It is preferable to present a Maxent map as a continuous gradient of relative suitability (52)

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(Available in S1 Supporting Information Fig 1) but we set a binary suitability threshold to better 266 summarize general patterns of gained, receded, and retained climate space (Fig 2). The TSS was between  We used the ML phylogeny to enforce clades for the southern, central, and northern lineages for 313 the BEAST2 analysis (Fig 3). Under a lognormal calibration prior, two of the three MCMC chains

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We were able to predict climate space into the Queretaro locality (the southern-most margin of the range) and where E. maculatum has been detected (71). Coincidently, the refugium is just southeast of Big Bend, 371 TX (Fig 1), which has been suggested as a "hotspot" locality for E. maculatum (22). Although specimens 372 from Cuatro Ciénegas Basin and Big Bend localities were unavailable for phylogenetic analysis, we 373 hypothesize that if this area was a refugium prior to expanding into the contemporary range, individuals northern CA, and ID specimens were unavailable in the current study, we were able to leverage the ENM 398 to reveal a potential route of early colonization through the Sierra Nevada and Cascade Mountain ranges 399 (Fig 2). This is based on the early divergence between northern and central lineages. E. maculatum 400 specimens are rare from CA but are known to occur along the two mountain chains from acoustic data 401 (25). Subsequent Holocene warming likely allowed the species to expand its range inwardly throughout 402 the Great Basin within the last six thousand years.

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Much uncertainty still surrounds the timing of the divergence between the central and northern 404 lineage because it was assumed from the fossil record and its placement was based on a partial phylogeny.