Efficient summary statistics for detecting lineage fusion from phylogeographic datasets

Abstract

Aim: Lineage fusion (merging of two or more populations of a species resulting in a single panmictic group) is a special case of secondary contact. It has the potential to counteract diversification and speciation, or to facilitate it through creation of novel genotypes. Understanding the prevalence of lineage fusion in nature requires reliable detection of it, such that efficient summary statistics are needed. Here, we report on simulations that characterized the initial intensity and subsequent decay of signatures of past fusion for 17 summary statistics applicable to DNA sequence haplotype data. Location: Global. Taxa: Diploid out-crossing species. Methods: We considered a range of scenarios that could reveal the impacts of different combinations of read length versus number of loci (arrangement of DNA sequence data), and whether or not pre-fusion populations experienced bottlenecks coinciding with their divergence (historical context of fusion). Post-fusion gene pools were sampled along 10 successive time points representing increasing lag times following merging of sister populations, and summary statistic values were recalculated at each. Results: Many summary statistics were able to detect signatures of complete merging of populations after a sampling lag time of 1.5 N e generations, but the most informative ones included two neutrality tests and four diversity metrics, with Z nS (a linkage disequilibrium-based neutrality test) being particularly powerful. Correlation was relatively low among the two neutrality tests and two of the diversity metrics. There were clear benefits of many short (200-bp × 200) loci over a handful of long (4-kb × 10) loci. Also, only the latter genetic dataset type showed impacts of bottlenecks during divergence upon the number of informative summary statistics. Main conclusions: This work contributes to identifying cases of lineage fusion, and advances phylogeography by enabling more nuanced reconstructions of how individual species, or multiple members of an ecological community, responded to past environmental change.

Population structure and phylogeography of three closely related tree peonies

“…Lineage fusion and splitting were probably caused by orogeny and climate change. Lineage fusion is a special case in which two or more populations of parental lineages that were not reproductively isolated collapse into a single lineage after they meet, which has an important impact on present‐day distributions of genetic diversity by reshuffling variation (Garrick et al, 2019 , 2020 ; Kearns et al, 2018 ). Lineage fusion events can be realized by horizontal gene transfer or hybridization (Niehus et al, 2015 ; Yue, Hu, et al, 2012 ).…”

Non-ultrametric phylogenetic trees shed new light on Neanderthal introgression

“…Nevertheless, the novel procedure can be generalized to all the cases of genetic recombination between populations/species, ranging from introgression to hybridization, from reticulation to repeated lineage splitting and lineage fusion, i.e. the complete merging of two or more populations resulting in a single panmictic group (Pickrell and Pritchard, 2012 ; Garrick et al, 2014 ; Hunley et al, 2016 ; Garrick et al, 2020 ). NUPT allows the prediction of the branching date between two populations/species when the amount of genetic material’s introgression is known.…”

Genetic signatures of lineage fusion closely resemble population decline

“…Statistical phylogeography requires that competing hypotheses make quantitatively different predictions about patterns of genetic variation, and that the true demographic history is represented within the set. Over the past decade there has been increasing interest in understanding what types of unique genetic signatures arise when isolated and populations come into secondary contact and fully merge back together (e.g., Alcala et al, 2013Alcala et al, , 2016Alcala & Vuilleumier, 2014;Garrick et al, 2019Garrick et al, , 2020. However, no study has assessed whether and when lineage fusion can be distinguished from decline.…”

“…Likewise, Garrick et al. ( 2019 , 2020 ) compared lineage fusion to size constancy and expansion‐contraction. In the present paper, we consider the term “lineage” broadly to include entities at and below the species‐level, but we focus on intraspecific lineages (i.e., long‐isolated population gene pools) as the basis of simulations that were used to explore the distinguishability of lineage fusion against a much broader suite of non‐fusion scenarios, focusing on six commonly used demographic history summary statistics (i.e., neutrality tests).…”

“…To obtain an appreciation of the prevalence of lineage fusion in nature, we need a better understanding of the circumstances under which these events produce recognizable genetic signatures and the potential for erroneously attributing these signatures to non-fusion processes (Garrick et al, 2019(Garrick et al, , 2020. In phylogeographic studies that employ statistical hypothesis testing, the basic units of analysis are usually local population gene pools, since these permit use of coalescent modeling (Hey & Machado, 2003).…”