Extending phylogeography to account for lineage fusion

Abstract

Secondary contact between long isolated populations has several possible outcomes. These include the strengthening of preexisting reproductive isolating mechanisms via reinforcement, the emergence of a hybrid lineage that is distinct from its extant parental lineages and which occupies a spatially restricted zone between them, or complete merging of two populations such that parental lineages are no longer extant ("lineage fusion" herein). The latter scenario has rarely been explicitly considered in single-species and comparative phylogeographic studies, yet it has the potential to impact inferences about population history and levels of congruence. In this paper, we explore the idea that insights into past lineage fusion may now be possible, owing to the advent of next-generation sequencing. Using simulated DNA sequence haplotype datasets (i.e., loci with alleles comprised of a set of linked nucleotide polymorphisms), we examined basic requirements (number of loci and individuals sampled) for identifying cases when a present-day panmictic population is the product of lineage fusion, using an exemplar statistical frameworkapproximate Bayesian computation. We found that with approximately 100 phased haplotype loci (each 400 bp long) and modest sample sizes of individuals (10 per population), lineage fusion can be detected under rather challenging scenarios. This included some scenarios where reticulation was fully contained within a Last Glacial Maximum timeframe, provided that mixing was symmetrical, ancestral gene pools were moderately to deeply diverged, and the lag time between the fusion event and gene pool sampling was relatively short. However, the more realistic case of asymmetrical mixing is not prohibitive if additional genetic data (e.g., 400 loci) are available.Notwithstanding some simplifying assumptions of our simulations and the knowledge gaps that remain about the circumstances under which lineage fusion is potentially detectable, we suggest that the recent release from data limitation allows phylogeographers to expand the scope of inferences about long-term population history.

Phylogeography of a cryptic speciation continuum in Eurasian spadefoot toads (Pelobates)

“…Sixth, the shallow phylogeographic lineages of P. b. balcanicus (<1 My) merged over hundreds of kilometers (Figure ), characteristic of lineage fusion (Garrick, Banusiewicz, Burgess, Hyseni, & Symula, ). These probably represent ephemeral divergences generated by glacial isolation, which are commonplace in the Balkans (e.g., Dufresnes et al, ).…”

Are glacial refugia hotspots of speciation and cytonuclear discordances? Answers from the genomic phylogeography of Spanish common frogs

“…Consequently, the delimitation of cryptic taxa has extensively relied on mitochondrial DNA (mtDNA) divergences (Krishnamurthy & Francis, 2012). However, it is now well established that deep mtDNA lineages do not always represent significant population divergences (Collins & Cruickshank, 2012;Morgan-Richards et al, 2017;Zink & Barrowclough, 2008), and even when they do, whether these kept diverging independently or faded away by recurrent episodes of admixture often remains an open question (Garrick, Banusiewicz, Burgess, Hyseni, & Symula, 2019).…”

“…A major issue with over-reliance on mtDNA is the prevalence of cytonuclear discordances across taxa (Bonnet, Leblois, Rousset, & Crochet, 2017;Toews & Brelsford, 2012), which can lead to false evolutionary and taxonomic conclusions ("mirage of cryptic species", Hinojosa et al, 2019). Cytonuclear discordances may have selective causes (local adaptation of mtDNA genes, Pavlova et al, 2013;asymmetric hybridization, Chan & Levin, 2005), but they often result from neutral demographic processes, e.g., faster rate of molecular evolution and lower effective sizes of mitochondrial DNA (Rosenberg, 2003), sex-biased dispersal (e.g., Dai, Wang, & Lei, 2013), or mitochondrial introgression or fusion following secondary contacts (e.g., Garrick et al, 2019;Phuong, Bi, & Moritz, 2017). Theoretical (Currat, Ruedi, Petit, & Excoffier, 2008;Excoffier, Foll, & Petit, 2009) and empirical data (Cahill et al, 2013;Phuong et al, 2017) have shown that demographic expansions at range margins can promote asymmetric gene flow in the initial stages of the contact (from the local to the expanding taxa), traces of which are expected to persist longer in the mitochondrial than in the nuclear genome.…”

Efficient summary statistics for detecting lineage fusion from phylogeographic datasets

“…Lineage fusion (merging of two or more populations of a species resulting in a single panmictic group) is a special case of the broader phenomenon of secondary contact (Garrick, Banusiewicz, Burgess, Hyseni, & Symula, 2019). While the term has been in use for over a decade (Campbell et al., 2008), the broader concept (i.e., including merging of reproductively isolated lineages) was described much earlier.…”

“…Rather than simply causing a net reduction in extant lineages, fission‐fusion dynamics may create new opportunities for selection, and subsequent diversification. Furthermore, if unrecognized, lineage fusion can mask the extent of similarity in which co‐distributed species responded to past environmental change (Garrick et al., 2019). By extension, lineage fusion can affect conclusions about the importance of biotic versus abiotic influences on phylogeographic structure (e.g., Garrick, Nason, Fernández‐Manjarrés, & Dyer, 2013; Satler & Carstens, 2017).…”