Reticulation, divergence, and the phylogeography-phylogenetics continuum

Abstract

Phylogeography, and its extensions into comparative phylogeography, have their roots in the layering of gene trees across geography, a paradigm that was greatly facilitated by the nonrecombining, fast evolution provided by animal mtDNA. As phylogeography moves into the era of next-generation sequencing, the specter of reticulation at several levels-within loci and genomes in the form of recombination and across populations and species in the form of introgression-has raised its head with a prominence even greater than glimpsed during the nuclear gene PCR era. Here we explore the theme of reticulation in comparative phylogeography, speciation analysis, and phylogenomics, and ask how the centrality of gene trees has fared in the next-generation era. To frame these issues, we first provide a snapshot of multilocus phylogeographic studies across the Carpentarian Barrier, a prominent biogeographic barrier dividing faunas spanning the monsoon tropics in northern Australia. We find that divergence across this barrier is evident in most species, but is heterogeneous in time and demographic history, often reflecting the taxonomic distinctness of lineages spanning it. We then discuss a variety of forces generating reticulate patterns in phylogeography, including introgression, contact zones, and the potential selection-driven outliers on next-generation molecular markers. We emphasize the continued need for demographic models incorporating reticulation at the level of genomes and populations, and conclude that gene trees, whether explicit or implicit, should continue to play a role in the future of phylogeography.

Keywords: coalescent theory; comparative phylogeography; introgression; monsoon tropics; species trees.

Fig. 1.

Diagram classifying the disciplines of population genetics, phylogeography, and phylogenetics. Traditionally, we think of these respective disciplines as being concerned with variation among organisms arising over short, intermediate, and long temporal (and often spatial) scales. Increasingly, with large quantities of data, there are opportunities to classify studies according to the way different processes are inferred to have shaped datasets. For example, it is likely that migration among populations is common in “population genetics” datasets and rarer in phylogenetics. Similarly, recombination is likely to reduce the detectable effects of linkage in population genetic datasets, such that the effects of linkage likely lead to larger haplotype blocks in studies at the “phylogeographic” scale. In this way, different studies might form, and next-generation methods might facilitate, a continuum from population genetics to phylogenetics. In this review, we focus on studies spanning the part of this continuum spanning phylogeography and shallow phylogenetics, indicated by the red box.

Fig. 2.

Sources of gene tree heterogeneity among diverging lineages. The three lineages KIM (K), TE, and CY are representative of northern Australia populations (Fig. 3). (A) These lineages are arranged by true evolutionary relationships depicted in gray: the “species” coalescent. (B) Within the species tree are gene trees colored in blue, yellow, red, and green. These gene trees represent independent coalescent histories and highlight various sources of gene tree discordance. Blue, green, and yellow gene trees highlight variation due to differing mutation rates and stochastic coalescent histories (including ILS), and red depicts effects of introgression among nonsister lineages. The MSC model allows for estimation of species trees, given mutational and coalescent variance. However, introgression, if extensive, can yield an incorrect species tree (e.g., [K, (TE,CY)] in this case) using most available methods. Additionally, distinguishing introgression from ILS in gene trees can be challenging and mostly relies on branch lengths in gene trees (as in IM models).

Fig. 3.

Gene tree heterogeneity in multilocus phylogeographic datasets of birds (Red-Backed Fairywren, Malurus melanocephalus; Poephila grassfinches; Climacteris treecreepers), skinks (Two-Spined Rainbow Skink, C. amax; Shaded-Litter Rainbow Skink, C. munda), and mammals (Petrogale rock-wallabies) across northern Australia. (A) Map of northern Australia showing the KTEB and CB that separate the KIM, TE, and CY faunas. (B) Cloudograms illustrate topological and branch length variation of gene trees. Violin plots represent the distribution of pairwise sequence divergences across the CB, and black dots indicate mean pairwise sequence divergence, or D_xy. Red dots and lines are estimates and 95% confidence intervals of population divergence across the KTEB, whereas green dots and lines are estimates and 95% confidence intervals of population divergence across the CB. (C) Distribution of rooted triplets shows that gene trees exhibiting deeper divergence times across the CB than the KTEB are the most frequent in all taxa except the Shaded-Litter Rainbow Skink. Additional details are provided in SI Text.

Fig. 4.

Contrasting processes and views of introgression. (A) Progression over time from population splitting, divergence in isolation, and secondary contact, with alternate outcomes: (i) tension zone, (ii) merging, and (iii) overriding of expanding population (blue) over the resident population with introgression from yellow→blue for some genes. (B and C) Contrasting perspectives on introgression among cryptic lineages of Australian Wet Tropics lizards at the local scale (B, contact zone) vs. lineage-scale estimates from IM analyses (modified from ref. 53). Note decreasing introgression at contact zones with increasing divergence time of lineage pairs, but no corresponding signal of decreasing migration at the lineage scale.