Wednesday, August 31, 2016

Network thinking in phylogeography?


This blog has, of course, long championed the importance of network models in phylogenetics. Slowly, very slowly, the rest of the world is catching up.

Apparently, the world of phylogeography has now woken up:
Scott V. Edwards, Sally Potter, C. Jonathan Schmitt, Jason G. Bragg and Craig Moritz (2016) Reticulation, divergence, and the phylogeography–phylogenetics continuum. Proceedings of the National Academy of Sciences of the USA 113: 8025-2032.
Phylogeography was conceived as some sort of connection between population biology and phylogenetics. It has always seemed odd that the tree model has been used in phylogeography at all, because there is no a priori reason to expect within-species phylogenetic patterns to be tree-like. Indeed, inter-breeding seems to suggest quite the opposite. Nevertheless, phylogeographic studies are full of trees.


But apparently no more. To quote the authors:
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 ... We 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 ...
That phylogeography sits centrally in this process-oriented space emphasizes the importance of understanding interactions between reticulation (gene flow / introgression and recombination), drift, and protracted isolation. This combination of processes sets phylogeography apart from traditional population genetics and phylogenetics.
Scanning entire genomes of closely related organisms has unleashed a level of heterogeneity of signals that was largely of theoretical interest in the PCR era. This genomic heterogeneity is profoundly influencing our basic concepts of phylogeography and phylogenetics, and indeed our views of speciation processes. It is now routine to encounter a diversity of gene trees across the genome that is often as large as the number of loci surveyed.
The new genome-scale analyses are causing evolutionary biologists to reevaluate the very nature of species, which, in some cases, appear to maintain phenotypic distinctiveness despite extensive gene flow across most of the genome, and to recognize introgression as an important source of adaptive traits in a variety of study systems.
The role of horizontal gene flow in speciation and phylogeography, particularly for animal taxa, has long been championed by Michael L. Arnold (see the references). However, the authors ignore this literature, and claim that this is a recent insight, instead. They also mention only in passing the extensive genomics literature on human introgression, where it is called "admixture". Indeed, they mention only a data-analysis technique, rather than the biological insights that have arisen. It is still disappointing just how little information-connection there is between different fields of biology.

Finally, the authors manage to mention the work "network" only three times in the whole paper. Their key word is "reticulation", instead, in the sense that a phylogeny is a tree with reticulation, rather than any other form of network. So, they are still only one step away from tree-thinking, and at least one step from true network-thinking.

In the context of trees versus networks, the authors mention so-called "species tree" methods based on the multispecies coalescent, which try to account for incomplete lineage sorting in genome studies (see also Edwards et al. 2016). Unfortunately, these have recently been shown to be inconsistent in the presence of gene flow (Solís-Lemus et al. 2016), thus emphasizing the need for proper network methods.

References

Arnold ML (1997) Natural Hybridization and Evolution. Oxford University Press.

Arnold ML (2006) Evolution Through Genetic Exchange. Oxford University Press.

Arnold ML (2009) Reticulate Evolution and Humans – Origins and Ecology. Oxford University Press.

Arnold ML (2016) Divergence With Genetic Exchange. Oxford University Press.

Edwards SV, Xi Z, Janke A, Faircloth BC, McCormack JE, Glenn TC, Zhong B, Wu S, Lemmon EM, Lemmon AR, Leaché AD, Liu L, Davis CC (2016) Implementing and testing the multispecies coalescent model: a valuable paradigm for phylogenomics. Molecular Phylogenetics & Evolution 94: 447-462.

Solís-Lemus C, Yang M, Ané C (2016) Inconsistency of species tree methods under gene flow. Systematic Biology 65: 843–851.