The Evolution of Comparative Phylogeography: Putting the Geography (and More) into Comparative Population Genomics

Abstract

Comparative population genomics is an ascendant field using genomic comparisons between species to draw inferences about forces regulating genetic variation. Comparative phylogeography, by contrast, focuses on the shared lineage histories of species codistributed geographically and is decidedly organismal in perspective. Comparative phylogeography is approximately 35 years old, and, by some metrics, is showing signs of reduced growth. Here, we contrast the goals and methods of comparative population genomics and comparative phylogeography and argue that comparative phylogeography offers an important perspective on evolutionary history that succeeds in integrating genomics with landscape evolution in ways that complement the suprageographic perspective of comparative population genomics. Focusing primarily on terrestrial vertebrates, we review the history of comparative phylogeography, its milestones and ongoing conceptual innovations, its increasingly global focus, and its status as a bridge between landscape genomics and the process of speciation. We also argue that, as a science with a strong "sense of place," comparative phylogeography offers abundant "place-based" educational opportunities with its focus on geography and natural history, as well as opportunities for collaboration with local communities and indigenous peoples. Although comparative phylogeography does not yet require whole-genome sequencing for many of its goals, we conclude that it nonetheless plays an important role in grounding our interpretation of genetic variation in the fundamentals of geography and Earth history.

Keywords: Gott Earth projection; indigenous knowledge; landscape genomics; place-based education; whole-genome sequencing.

Fig. 1.

Number of publications per year with some variant of “comparative phylogeography” in the title, as referenced in the InCite database (accessed March 28, 2021). Dashed red line indicates a line of constant increase in numbers of publications from 1999 to 2008 (slope, increase of 6.42 publications per year). Dashed bar for 2021 indicates that a partial year is represented. Data are from the 1229 articles in supplementary tables S1 and S2, Supplementary Material online.

Fig.2

Major sites of comparative phylogeographic exploration in the New World, on a map with the new Gott et al. (2021) projection, which minimizes 2D distortion and orientation of landmasses less so than any previous projection. Numbers correspond to listings in supplementary table S4, Supplementary Material online.

Fig. 3.

Major phylogeographic breaks in the Old World, with projection details as in figure 2. Numbers correspond to listing of breaks in supplementary table S4, Supplementary Material online.

Fig. 4.

Global trends in geographic locations of authors of publications in comparative phylogeography in two time periods, 1992–2008 and 2009–present. (A) Proportion of publications with authors from countries listed on the x-axis to total publication output for two time periods. (B) Shifts in number of publications and proportion of publication by authors in countries listed as Global North or Global South (country designations from https://meta.wikimedia.org/wiki/List_of_countries_by_regional_classification). Data on which these figures are based are in supplementary table S3, Supplementary Material online. We recognize that the terms “Global North” and “Global South” may offend some readers and for that we apologize.

Fig. 5.

Depiction of how different approaches in comparative genetics scale geographically. In this example, focused on low dispersal vertebrates northern Australia, population to landscape studies might be done in the north Kimberly at scales of 10–200 km, phylogeographic to speciation studies at the scale of 100s—1000 km (Kimberley to Top End), and speciation to macroevolution at continental scale. Images are from Google Earth; see Potter et al. (2018) as an example.