Assembly of the Great Lakes Flora and Vegetation

Geological Timeline: moving onto land and to the Great Lakes Assembly of the Great Lakes Flora and Vegetation

. . . Pleistocene refugia and the Holocene . . .

Pleistocene & Holocene Climate Pleistocene & Holocene Climate

Wisconsin Holocene • Younger Dryas !

Dryas (Rosaceae) temperature 12,000 ya

St. Lawrence Seaway exposed for 10.5-12 Kya cold melt water runoff

1 Pleistocene Refugia ? Pleistocene Refugia ?

• Extensive boreal forest zone S to 33°N Presence of survivia or refugia of these plants and animals south of the ice has been a major contention — are there consistent areas of refuge • Mixed deciduous forest zone near Gulf during the Pleistocene?

• 18,000 ya harshest conditions; zones were further north earlier

18,000 ya 28 - 25,000 ya

Pleistocene Refugia ? Pleistocene Refugia ?

Presence of survivia or refugia of these plants and animals south of the ice has been a major contention — are there consistent areas of refuge during the Pleistocene? 2008 – Molecular Phylogenetics and Evolution

Ginkgo fossil from Washi ngt on, USA – 49 mya

Yes - plant and animal phylogeographic studies provide congruent areas of centers of genetic diversity in Europe Ginkgo, now confined to China, had a wide Holarctic distribution from the Paleocene into the Neogene as indicated by fossil localities (=)

2 Pleistocene Refugia ? Pleistocene Refugia ?

Is there genetic evidence of a Pleistocene refugium?

1,400 year old Ginkgo in Gu Guanyin Buddhist Temple in the Zhongnan Mountains, China

Ginkgo “native” distribution in China and “introduced” AFLP variation indicates two strongly differentiated set of populations – distribution in Japan southwestern China and east-central China

Pleistocene Refugia ? Pleistocene Refugia ?

Is there genetic evidence of a Pleistocene refugium? Is there genetic evidence of a Pleistocene refugium? Is there genetic evidence of human movement to Japan and later the world?

Japan & the world

AFLP and cpDNA haplotypes indicate two refugia – southwestern China Haplotype E is the only Chinese haplotype found in Japan and the rest of the and east-central China world – derived originally from east-central China

3 RESEARCH ARTICLE Pleistocene Refugia ? Pleistocene Refugia ?

394 • American Journal of Botany RADseq genetic structure analysis Phylogeography of a widespread eastern North American A C shrub, Viburnum lantanoides • south - Appalachian Brian Park1,2,3 and Michael J. Donoghue1 American Journal of Botany 2019 • north – mostly glaciated

Manuscript received 5 July 2018; revision accepted 10 December PREMISE OF THE STUDY: There have been relatively few phylogeographic studies of eastern 2018. North American plants, especially of animal- dispersed shrubby species, and this leaves a 1 Department of Ecology and Evolutionary Biology, Yale University, signifcant gap in our understanding of how such species were afected by glacial events. P.O. Box 208106, New Haven, Connecticut 06520, USA Here, we analyzed the phylogeography of the widespread understory shrub Viburnum 2 Current address: Department of Plant Biology, University of lantanoides. Georgia, Miller Plant Sciences Building, Athens, Georgia 30602, USA 3 Author for correspondence (e-mail: [email protected]) METHODS: We generated RADseq data and paleoclimatic species distribution models Citation: Park, B. and M. J. Donoghue. 2019. Phylogeography of a (SDMs) to identify the locations of refugia where V. lantanoides may have survived the Last widespread eastern North American shrub, Viburnum lantanoides. Glacial Maximum (LGM) and how its range expanded as glaciers receded. American Journal of Botany 106(3): 389–401. KEY RESULTS: Genetic diversity falls of with increasing latitude and longitude, indicating doi:10.1002/ajb2.1248 that range expansion likely occurred via serial founder events from southern source B D populations. Samples from the southern Appalachians form a grade, while those from the north form a clade, suggesting that a single genetic lineage recolonized the north. SDMs indicate that V. lantanoides probably survived the LGM in refugia on the mid- Atlantic Coastal Plain and/or the interior Gulf Coastal Plain.

CONCLUSIONS: Our analyses indicate that V. lantanoides survived the LGM in refugia south 396 • American Journal of Botany of the glacier but north of the extensive refugium along the Gulf Coast. Following the LGM, a single population expanded northward along the Appalachian Mountains and eventually into eastern Canada. The patterns observed here suggest that range expansion occurred TABLE 1. Maximum- likelihood estimates and 95% confdence intervals (CI) of population sizes and divergence times for Viburnum lantanoides inferred through in a stepwise manner, similar to postglacial dynamics observed in a number of European demographic reconstruction. N1 refers to the southern Appalachian cluster; N2 refers to the northern lineage. plant species. Nref (10 3 ) N1 (10 3 ) N2 (10 3 ) T (10 3 yr) KEY WORDS eastern North America; Last Glacial Maximum; RADseq; species distribution Model AIC ΔAIC Log- likelihood (95% CI) (95% CI) (95% CI) (95% CI) models. (A) No size change 818 20.0 −405 26.1 12.7 6.13 38.2 (24.6–27.6) (9.76–15.7) (4.70–7.55) (33.7–42.7) (B) Size change in N1 810 12.3 −401 26.1 7.86 6.27 39.3 (24.7–27.5) (5.20–10.5) (5.86–6.68) (35.1–43.5) (C) Size change in N2 806 8.43 −399 25.7 14.1 3.14 44.5 (24.4–27.0) (11.6–16.6) (2.73–3.55) (40.8–48.2) Repeated episodes of glacial expansion and retreat, most recently refugia characterized by long- distance dispersal and founder events FIGURE 2. Population structure of Viburnum lantanoides. (A) Map depicting the distribution of ancestry coefcients inferred through tess3r for (D) Size change in N1 and N2 798 0 −395 25.7 9.33 3.23 45.6 K = 2 clusters. Sampling localities are represented by black dots. More saturated colors indicate a greater proportion of ancestry to either cluster. (B) during the Last Glacial Maximum (LGM; ~21,500 ybp), have had a (Hewitt, 1999, 2000). Some European species have been found to (24.4–27.0) (6.72–11.9) (2.95–3.52) (41.8–49.3) signifcant impact on the evolutionary histories of plant species in be most genetically diverse at midlatitudes, which may be a conse- Individual admixture coefcients at K = 2 clusters inferred using sNMF, tess3r, and DAPC. PCA plots of the frst and second (C) and of the frst and third the temperate Northern Hemisphere (Hewitt, 2000, 2004). Regional quence of secondary contact between isolated populations originat- (D) principal components show that samples cluster by geography and that there is not a clear gap between southern Appalachian and northern phylogeographic studies have been instrumental in identifying sim- ing from separate southern refugia (Petit, 2003). In Eastern Asia, by populations. ilarities and diferences in how species responded to these events. contrast, climatic conditions during the LGM were less severe, and southern portion of the range (Fig. 3). Furthermore, high support ENA species (e.g., Schwaegerle and Schaal, 1979; Broyles, 1998; Tese have provided important insights into the locations of refu- many temperate forest species may have survived the LGM more current- day southernfor a demographic Arkansas, Mississippi, model with northern population Louisiana, expansion/contraction with increasing distanceZinck from and Rajora,the southern 2016), portion though of some the geoENA- species appear to lack gia where species persisted during glacial periods and the modes of or less in place, perhaps in multiple refugia distributed throughout and eastern Texasin in the the northern interior Gulf lineage Coastal (Appendix Plain (Fig. S2D; 4C). Table With 1) andgraphic the threefold range (Fig. 1B,a clear C). clinalSamples pattern sorted in into genetic one diversitygenetic clus (e.g.,- Lumibao et al., 2017; postglacial range expansion that explain the distribution of genetic their contemporary ranges (e.g., Hu et al., 2008; Tian et al., 2009; MPI, suitable climatesdiference were in identi efectivefed in population both the Atlantic size estimated Coastal betweenter including the south the- southernBemmels Appalachian and Dick, populations 2018). Tis and may another refect the relatively simple diversity over their contemporary geographic ranges. Bai et al., 2010; Zeng et al., 2015). In western North America, the Plain and in theern Gulf Appalachian Coastal Plain cluster in and Arkansas the northern and northern lineage (~9000one including vs. ~3000; the northernlandscape populations and mild glacial (Fig. history2A–D). ofHowever, ENA as compared with Europe A number of important phylogeographic patterns have emerged complex physiography of the region combined with the presence of Louisiana (Fig. 4D).Table Despite 1) signal these that di frangeerences, expansion all models was indicate accompanied overall by populationthe loss structure(Hewitt, 2000;was di Shaferfuse andet al., the 2010; proportion Qiu et al., of 2011), which may have from these studies. In Europe, where climatic conditions were es- large refugia in Beringia and the Pacifc Northwest, as well as small that V. lantanoidesof genetic survived diversity. the LGM in a southern refugium, be- southern Appalachianenabled ancestry some decreased species—especially steadily with wide-increasranging, - wind- pollinated pecially harsh during the LGM, many temperate forest species refugia on coastal islands, has generated north-south, south- north, low the southern extentOverall, of the V. Laurentide lantanoides Ice Sheet. follows the classic phylogeographicing latitude and decreasingtrees—to longitude. have survived Tese resultsthe LGM strongly in large sup -numbers over wide ar- exhibit declines in genetic diversity at higher latitudes,Pleistocene which has and east- west patterns of geneticRefugia diversity and population structure? pattern of “southern diversity,Pleistocene northern purity” observedport a patternin many ofRefugia IBD.eas, Samples and to havefrom expandedthe southern? their Appalachian ranges gradually along a contin- been explained by northward range expansions from southern (Brunsfeld et al., 2001; Shafer et al., 2010). European temperate forest species (Hewitt, 1999, 2000,region 2004; were Petit, found touous form migration a grade while front. samples Tis mode from ofnorth postglacial of range expansion DISCUSSION 2003). Tis pattern has also been demonstrated inthis a region number formed of awould well-supported serve to preserve clade (Fig. genetic 3), suggesting diversity that and maintain connectivity March 2019, Volume 106 • Park and Donoghue—Phylogeography of hobblebush • 395 a single genetic lineage may have colonized the northern portion We reconstructed the postglacial migration history of V. lan- of the range of V. lantanoides. Te genetic diferentiation of the north tanoides using recentlyA developed genomic tools and paleocli- southern AppalachianB lineages from the northern lineage was in- American Journal of Botany 106(3): 389–401, 2019; http://www.wileyonlinelibrary.com/journal/AJB © 2019 Botanical Society of America • 389 matic distribution modeling. We identifed a signifcant pattern ferred to have occurred prior to the LGM, with all having under- of IBD (Fig. 1A) and found that genetic diversity declined steadily gone signifcant reductions in efective population size following

present 20 kya south

C D

northern populations derived out of southern populations 20 kya 20 kya

FIGURE 4. Species distribution models for Viburnum lantanoides inferred using Maxent. (A) Current climatic conditions. (B–D) Projections into LGM climate models: (B) CCSM4, (C) MIROC- ESM, and (D) MPI- ESM- P. Blue areas denote ice- covered areas during the LGM. Species distribution models

FIGURE 3. Phylogram depicting relationships among samples inferred through RAxML suggests that a single genetic lineage recolonized the northern portion of the range of Viburnum lantanoides. Red tips denote samples with a high proportion of southern Appalachian ancestry as inferred through population structure analyses; blue tips denote samples with a high proportion of northern ancestry; white tips denote “admixed” samples with nearly equal proportions of southern Appalachian and northern ancestry. Tip labels refer to the state or province the sample was collected in. All nodes were resolved with >90 bootstrap support.

the origination of the northern lineage (Table 1). Finally, using population structure (Fig. 2A–D) suggest that genetic variation paleoclimate distribution modeling, we found that V. lantanoides is continuously distributed across the range of V. lantanoides. underwent major range displacement during the LGM, and likely However, genetic variation was found to decrease predictably with survived in refugial areas on the Atlantic Coastal Plain or the in- increasing distance from the southern edge of its range (Fig. 1B, terior Gulf Coastal Plain or both (Fig. 4). Taken together, these C), indicating that recolonization occurred in a northward and 4 analyses imply that V. lantanoides survived glacial periods in one then eastward direction from source populations in the southern or more southern refugia and then expanded its range into the Appalachians. Tese patterns are suggestive of V. lantanoides hav- southern Appalachian Mountains and then northward and ulti- ing undergone a “stepping- stone” mode of postglacial range expan- mately eastward, in a series of founder events accompanied by the sion (Sage and Wolf, 1986; Broyles, 1998), where recolonization of loss of genetic diversity. previously glaciated areas occurred through serial founder events along a single migration front, each of which drew propagules from Postglacial range expansion an increasingly limited pool of genetic diversity. Several lines of evidence support this scenario. Phylogenetic Signifcant IBD (Fig. 1A), moderate population diferentiation resolution of a southern Appalachian grade and a well-supported

(Fst = 0.186), and an absence of strong geographic breaks in northern clade indicates that a single lineage dispersed out of the Assembly of Great Lakes Flora Assembly of Great Lakes Flora

How did the assembly of flora and vegetation in the Great Lakes happen? Yearly deposits accumulate in lake bottoms to be covered by silt in layers, or in bog peat strata

18,000 ya Present

Assembly of Great Lakes Flora Assembly of Great Lakes Flora Shifts of vegetation belts Coniferous species migrated into the starting at about 13,000 ya with Great Lakes region in waves: tundra, spruce, pine, northern Boreal species like spruce, tamarack, hardwood, pine-oak, and then and balsam fir arrived first boreal oak-hickory tundra spruce- pine

pine- spruce- hardwood oak- hickory mixed hardwood

5 Assembly of Great Lakes Flora Assembly of Great Lakes Flora Coniferous species migrated into the Coniferous species migrated into the Great Lakes region in waves: Great Lakes region in waves: Boreal species like spruce, tamarack, Boreal species like spruce, tamarack, and balsam fir arrived first and balsam fir arrived first

Assembly of Great Lakes Flora Assembly of Great Lakes Flora Coniferous species migrated into the Coniferous species migrated into the Great Lakes region in waves: Great Lakes region in waves: Xeric pine species like jack pine and . . . followed by more mesic white red pine arrived next pine

6 Assembly of Great Lakes Flora Assembly of Great Lakes Flora Coniferous species migrated into the Angiosperm trees migrated into the Great Lakes region in waves: Great Lakes region in waves towards the end of conifer migration: Hemlock, characteristic of mesic Northern Hardwood forests, arrived Oaks, hickories and elms arrived last first - 11,000 ybp

Assembly of Great Lakes Flora Assembly of Great Lakes Flora Angiosperm trees migrated into the Angiosperm trees migrated into the Great Lakes region in waves towards Great Lakes region in waves towards the end of conifer migration: the end of conifer migration: Followed by mesic-loving maples And finally American beech last

7 Pleistocene Refugia ? Pleistocene Refugia ? Importantly, the different species of trees (and herbs) entering the Great Importantly, the different species of trees (and herbs) entering the Great Lakes region after the glaciers retreated entered via different routes - that Lakes region after the glaciers retreated entered via different routes - that is, they came from different refugia or survivia south of the ice is, they came from different refugia or survivia south of the ice

pollen record pollen record (Kya) (Kya)

Ozarkian Alleghenian

White pine from the Alleghenian Oaks from either the Alleghenian (white oak) or Ozarkian refugium and present distribution (bur oak) refugia and present overlapping distributions

Pleistocene Refugia ? Assembly of Great Lakes Flora The assembly of Holocene flora in northern Europe, especially Great The flora of the Great Lakes can be divided into a number of elements, Britain, shows a similar pattern to that in eastern North America each of which shares a common geographical origin.

elm alder Closely related species (such as oaks) can often be part of different floristic elements. This is due to both different ecological preferences (such as fast migration hydric vs. mesic vs. xeric) and to geographical origin.

beech

slow migration Quercus - the oaks

8 Assembly of Great Lakes Flora Assembly of Great Lakes Flora

The flora of the Great Lakes can be divided into a number of elements, each of which shares a common geographical origin.

1. Alleghenian: group of species with ranges centered from 1. Alleghenian: Cumberland and Great Smoky mountains; dominant in deciduous forests; e.g. white pine, hemlock and basswood; ancient element extending back to the Tertiary Fagus grandifolia - American beech

Tilia americana - basswood

Pinus strobus - white pine Tsuga canadense - hemlock Acer sacccharum - sugar maple Quercus alba - white oak

Assembly of Great Lakes Flora Assembly of Great Lakes Flora

The flora of the Great Lakes can be divided into a number of elements, Jeff Rose’s pictures from field trip each of which shares a common geographical origin.

1. Alleghenian:

2. Ozarkian: species grouped around the Ozark Mts. of Arkansas and Missouri; more adapted to xeric or dry Dicentra cucullaria - Dutchman’s breeches conditions, but similar to Alleghenian (many genera, but not species overlapping between the two elements); e.g. bur oak and black oak, hickory Erythronium albidum – trout lily Quercus macrocarpa Carya ovata Bur oak Shagbark hickory Claytonia virginiana - spring beauty

9 Assembly of Great Lakes Flora Assembly of Great Lakes Flora

The flora of the Great Lakes can be divided into a number of elements, each of which shares a common geographical origin.

2. Ozarkian: 3. Prairie: species whose ranges includes all or part of existing prairies e.g. needle grass, side oats

Phlox divaricata Blue phlox

Anemonella thalictroides Rue anemone Silphium intregiifolium - silphium

Assembly of Great Lakes Flora Assembly of Great Lakes Flora

Andropogon gerardii big bluestem

3. Prairie: 3. Prairie:

ArctoTertiary element in prairies

Anemone patens Pasque flower Amorpha canadense - leadplant (photo: John Zabosky– Apr 27. 13)

10 Assembly of Great Lakes Flora Assembly of Great Lakes Flora

The flora of the Great Lakes can be divided into a number of elements, each of which shares a common geographical origin.

Pyrola rotundifolia Round-leaved shinleaf

4. Boreal: species w/ranges from Larix laricina 4. Boreal: Alaska to Upper Great Lakes, many Larch, tamarack species circumboreal (with ranges in Iris lacustris Eurasia) e.g. tamarack, white spruce, Dwarf-lake iris and balsam fir

Abies balsamea Balsam fir

Picea glauca White spruce Linnaea borealis - twinflower

Assembly of Great Lakes Flora Assembly of Great Lakes Flora

The flora of the Great Lakes can be divided into a number of elements, each of which shares a common geographical origin. Chamaesyce polygonifolia Seaside spurge

5. Coastal Plain: species with 5. Coastal Plain: . . . and including distributions originating from the coastal species inhabiting water edges of the plain region of SE United States . . . Great Lakes and maritime regions of the Coastal Plain

Betula nigra River birch

Gledistia tricanthos Honey locust

11 Assembly of Great Lakes Flora

Lathyrus japonicus Beach pea

5. Coastal Plain: . . . and including species inhabiting water edges of the Great Lakes and maritime regions of the Coastal Plain Coastal Plain Marsh

Sandy to peaty-mucky lakeshores, pondshores, depressions, and ditches in and around the bed of extinct glacial Lake Wisconsin may harbor assemblages of wetland species including some which are significantly disjunct from their main ranges on the Atlantic Coastal Plain. There is often a well-developed concentric zonation of vegetation. Frequent members of this community are sedges in the genera Cyperus, Eleocharis, Fimbristylis, Hemicarpha, Rhynchospora and Scirpus; rushes (Juncus spp.); milkworts (Polygala cruciata and P. sa n g u in e a ), toothcup (Rotala ramosior), meadow-beauty (Rhexia virginica), grass-leaved goldenrod (Euthamia graminifolia), hardhack (Spiraea Cakile edulenta tomentosa), lance-leaved violet (Viola lanceolata), and yellow-eyed grass (Xyris torta). Sea rocket

Assembly of Great Lakes Flora Assembly of Great Lakes Flora

The flora of the Great Lakes can be divided into a number of elements, each of which shares a common geographical origin.

6. Western North America: species 6. Western North America: with a primary western North America Essentially a variety or distribution and disjunct occurrence in subspecies of the western the Great Lakes region A. columbianum

Aconitum noveboracense Dasiphora fruticosa ’ Northern monk s-hood Shrubby cinquefoil

12 Assembly of Great Lakes Flora Assembly of Great Lakes Flora

6. Western North America: 6. Western North America:

Note that the distribution in the east is north of glacial maximum • western distribution spans both glaciated and unglaciated regions • eastern distribution confined to glaciated regions

Dasiphora fruticosa Shrubby cinquefoil Shepherdia canadensis Buffalo-berry

Assembly of Great Lakes Flora Assembly of Great Lakes Flora

6. Western North America: 6. Western North America:

Note that the distribution in the east is Note that a close eastern relative is not north of glacial maximum confined to glacial regions

Actaea rubra Actaea pachypoda Red baneberry White baneberry

13 Assembly of Great Lakes Flora Assembly of Great Lakes Flora

6. Western North America: 6. Western North America:

Basically confined to glacial regions despite available sites in Driftless Region A number of western elements are completely disjunct between Alaska (unglaciated areas) and sandy areas of the Great Lakes (beaches, sand outwash)

or with sporadic occurrence in Dakotas, Wyoming, Alberta

Typical western North America — Besseya bullii Great Lakes pattern Kitten’s-tail (Muralt Bluff Prairie)

Assembly of Great Lakes Flora Assembly of Great Lakes Flora Species migrating into the Great Lakes region not only came from different places and at Species restricted to beaches of Great Lakes and different rates, but also ended up in specific regions and associated with specific groups. into Maritime region of eastern Canada. Hulten considered it as a subspecies of the Alaskan and 6. Western North America: Pacific Northwestern species T. bipinnatum. Two major biotic associations exist in the Great Lakes region:

1. northern hardwood- conifer forest

Tanacetum huronense Lake Huron Tansy

14 Assembly of Great Lakes Flora Assembly of Great Lakes Flora Species migrating into the Great Lakes region not only came from different places and at Species migrating into the Great Lakes region not only came from different places and at different rates, but also ended up in specific regions and associated with specific groups. different rates, but also ended up in specific regions and associated with specific groups.

Two major biotic associations Two major biotic associations exist in the Great Lakes region: exist in the Great Lakes region:

1. northern hardwood- 1. northern hardwood- conifer forest conifer forest

2. eastern deciduous forest 2. eastern deciduous forest

These two associations are separated by a fairly sharp tension line or zone

Assembly of Great Lakes Flora Assembly of Great Lakes Flora

The tension zone is quite The tension zone separating the two provinces is based on the upper and lower obvious just by looking at distributional limits of the southern and northern species, respectively. a pre-settlement vegetation map of Wisconsin

In Wisconsin the two areas are often referred to as two floristic provinces:

• Northern Hardwoods

• Prairie-Forest

’ Golden cassia Wild indigo Ram s head Stemless ladyslipper ladyslipper

15 Assembly of Great Lakes Flora Assembly of Great Lakes Flora

Within each province, there are ecological (not floristic) assemblages of species called plant communities. John Curtis in the Vegetation of A compilation of the range Wisconsin, described about 35 communities (the subject of Botany 455). limits (northern or southern) of 182 species in Wisconsin shows species range limits per county

Tension zone

Vascular Flora of Wisconsin . . . Vascular Flora of Wisconsin . . . after the assembly . . . after the assembly . . .

Information source: Wisconsin State Herbarium www.botany.wisc.edu/herbarium/

Arethusa bulbosa Dragon’s mouth Native species = 1889

Alliaria petiolata Garlic mustard Introduced species = 681

158 families 758 genera 2570 species