Comparative phylogeography clarifies the complexity and problems of continental distribution that drove A. R. Wallace to favor islands

Abstract

Deciphering the geographic context of diversification and distributional dynamics in continental biotas has long been an interest of biogeographers, ecologists, and evolutionary biologists. Thirty years ago, the approach now known as comparative phylogeography was introduced in a landmark study of a continental biota. Here, I use a set of 455 studies to explore the current scope of continental comparative phylogeography, including geographic, conceptual, temporal, ecological, and genomic attributes. Geographically, studies are more frequent in the northern hemisphere, but the south is catching up. Most studies focus on a Quaternary timeframe, but the Neogene is well represented. As such, explanations for geographic structure and history include geological and climatic events in Earth history, and responses include vicariance, dispersal, and range contraction-expansion into and out of refugia. Focal taxa are biased toward terrestrial or semiterrestrial vertebrates, although plants and invertebrates are well represented in some regions. The use of various kinds of nuclear DNA markers is increasing, as are multiple locus studies, but use of organelle DNA is not decreasing. Species distribution models are not yet widely incorporated into studies. In the future, continental comparative phylogeographers will continue to contribute to erosion of the simple vicariance vs. dispersal paradigm, including exposure of the widespread nature of temporal pseudocongruence and its implications for models of diversification; provide new templates for addressing a variety of ecological and evolutionary traits; and develop closer working relationships with earth scientists and biologists in a variety of disciplines.

Keywords: biodiversity conservation; biogeography; diversification; ecology; evolutionary biology.

Fig. 1.

(A) Six terrestrial biogeographic regions of the world, basically dating to Wallace (2), but this depiction (map modified with permission from ref. 4) with boundaries modified modestly and with proposed subregions (see original paper for additional terminology). Numbers refer to distribution of comparative phylogeographic studies of continental biotas using references database described further in text. (B) Growth of continental comparative phylogeographic studies 1992–2015, total and tabulated by biogeographic region using references database described further in text (numbers for 2015 not complete because database was downloaded from Web of Science in December 2015).

Fig. 2.

Anatomy and life history of an idealized focal system in continental comparative phylogeography. A focal system is defined here as one that generates repeated studies, each time adding new taxa and/or new genomes/genetic markers.

Fig. 3.

Continental comparative phylogeography hotspots or emerging hotspots (replicate studies using cumulatively increasing numbers of taxa) as inferred from scan of references database used here. Each set of colored dots represent a biogeographic region, except for those numbers that represent transition zones between regions: 36, OR-PA, Eastern Himalayas/Qunghai-Tibet Plateau; 37, ET-PA, Mediterranean Basin; 38, NT-NE, Middle America; 39, PA-NA, Beringea. All other localities identified as follows: 1, Alaska/East Beringea; 2, Pacific Northwest; 3, California; 4, Rocky Mountains; 5, Southwestern Aridlands; 6, Southeastern/Eastern; 7, Trans Mexican Volcanic Belt; 8, European Alps/Carpathians; 9, Western Palearctic; 10, Balkan Peninsula; 11, Eastern Asia; 12, Eurasia; 13, Italian Peninsula; 14, Iberian Peninsula; 15, Central Asia/Ponto-Caspian; 16, Australian Wet Tropics; 17, Interior Deserts; 18, Southwestern Australia; 19, Pilbara Region; 20, Monsoonal Tropics; 21, Souteastern Australia/Tallaganda; 22, Endorheic Basins; 23, Southern Australia; 24a, Lower Central American lowlands; 24b, Lower Central American highlands; 25, trans-Andean; 26, Andes; 27, Patagonia; 28, Amazon Rain Forest; 29, Caatinga/Cerrado; 30, Atlantic Rain Forest; 31, Eastern Arc (Afromontane) Mountains; 32, Central African Forest; 33, West African Forests/Savannas; 34, Cape Region; 35, Tropical African Forests/Savannas. Map modified with permission from ref. .

Fig. 4.

Frequency of terms generated through searches of references database used here, embedded within six categories (A–F) considered here to represent a range of primary foci of continental comparative phylogeography. Those followed by an asterisk denote root terms that find any variation (e.g., allopat* will find allopatric, allopatry, allopatrically). The total frequencies of the six primary foci (G and H) differ because the latter was generated after removing three terms of overriding frequency, showing a more even distribution across the primary foci.

Fig. 5.

The timeframes explored empirically by continental comparative phylogeography. Terms used to describe geological timeframes differ among studies (A) but are subsumed for purposes of searching the reference database as Neogene (=Miocene + Pliocene) and Quaternary (=Pleistocene + Late Glacial/post Glacial + LGM + Holocene). Late Cenozoic global climate trend traced from an online summary (www.columbia.edu/∼mhs119/Sensitivity+SL+CO2/) of a well-known figure (27). Studies using terms describing timeframes (total numbers tallied for each region overlaid on pie charts) summarized as (B) late Glacial/post Glacial vs. Quaternary all, and (C) Neogene only vs. Quaternary only vs. Neogene and Quaternary. Map modified with permission from ref. .

Fig. 6.

(A and B) Categories referenced frequently in continental comparative phylogeography of biotic responses to geological and climatic events (total numbers tallied for each region overlaid on pie charts). Studies divided to contrast terms (A) vicariance only vs. dispersal only vs. vicariance + dispersal, and (B) refugia only vs. range dynamics only vs. refugia + range dynamics. Range dynamics includes references to range expansion, range contraction, and range shift and variants of each. (C and D) Frequencies of organisms, summarized into taxonomic groups and medium inhabited, studied in continental comparative phylogeography according to search of the database used in this study. Taxa contrasted (C) as vertebrate vs. invertebrate vs. plants vs. fungi; and medium (D) contrasted as terrestrial or semiaquatic vs. aquatic organisms. (E and F) Frequencies of genomes used in continental comparative phylogeography studies. Organelle DNA (including mitochondrial DNA and chloroplast DNA, also searched as mtDNA and cpDNA) contrasted (E) with nuclear DNA (including all types of markers) as organelle only vs. nuclear only vs. organelle and nuclear. The frequency of studies (F) using markers from each genome plotted through time (numbers for 2015 not complete because database was downloaded from Web of Science in December 2015). Map modified with permission from ref. .

Fig. 7.

Positioning of continental comparative phylogeography within a depiction of related disciplines across spatial, temporal, and scale of pattern/process hierarchies.