Species delimitation with gene flow: A methodological comparison and population genomics approach to elucidate cryptic species boundaries in Malaysian Torrent Frogs

Abstract

Accurately delimiting species boundaries is a nontrivial undertaking that can have significant effects on downstream inferences. We compared the efficacy of commonly used species delimitation methods (SDMs) and a population genomics approach based on genomewide single-nucleotide polymorphisms (SNPs) to assess lineage separation in the Malaysian Torrent Frog Complex currently recognized as a single species (Amolops larutensis). First, we used morphological, mitochondrial DNA and genomewide SNPs to identify putative species boundaries by implementing noncoalescent and coalescent-based SDMs (mPTP, iBPP, BFD*). We then tested the validity of putative boundaries by estimating spatiotemporal gene flow (fastsimcoal2, ABBA-BABA) to assess the extent of genetic isolation among putative species. Our results show that the A. larutensis complex runs the gamut of the speciation continuum from highly divergent, genetically isolated lineages (mean F = 0.9) to differentiating populations involving recent gene flow (mean F = 0.05; N > 5). As expected, SDMs were effective at delimiting divergent lineages in the absence of gene flow but overestimated species in the presence of marked population structure and gene flow. However, using a population genomics approach and the concept of species as separately evolving metapopulation lineages as the only necessary property of a species, we were able to objectively elucidate cryptic species boundaries in the presence of past and present gene flow. This study does not discount the utility of SDMs but highlights the danger of violating model assumptions and the importance of carefully considering methods that appropriately fit the diversification history of a particular system.

Social but lonely: Species delimitation of social voles and the evolutionary history of the onlyMicrotusspecies living in Africa

“…The molecular delimitation of Microtus species may be more accurate with the use of a less subjective framework, such as the GMYC species delimitation model recently applied to determine the species of Chinese voles (Liu et al, 2017) or the mPTP model applied here for the first time in voles. We find the mPTP model to be the most appropriate species delimitation tool for this study system, since it is (a) stable across sampling regimes, (b) not overly conservative, as GMYC may be and (c) resistant to "over-splitting", meaning that it does not overestimate species in the presence of marked population structure and gene flow (Blair & Bryson, 2017;Chan et al, 2017;Kapli et al, 2017). Finally, it may be preferable in datasets with highly uneven sampling or large differences in effective population sizes of species (Blair & Bryson, 2017).…”

Genomic data reveal deep genetic structure but no support for current taxonomic designation in a grasshopper species complex

“…However, integrative species delimitation approaches are not exempt of limitations (Huang, ; Sukumaran & Knowles, ). One of these limitations is the challenge to deal with sexually dimorphic traits (Solis‐Lemus et al, ), which can have a considerable impact on species delimitation inferences (Chan et al, ; Noguerales, Cordero, & Ortego, ). More importantly, the finest detection of genetic differentiation brought by the highest resolution of genomic data can lead to a potential confusion of population genetic structure with species boundaries (Carstens, Pelletier, Reid, & Satler, ; O'Meara, ; Sukumaran & Knowles, ).…”

Phylogeography and Molecular Species Delimitation Reveal Cryptic and Incipient Speciation in Synchronous Flashing Fireflies (Coleoptera: Lampyridae) of Southeast Asia

“…However, based on the relatively shallow divergences among populations from PM and Borneo, we hypothesize that cyclical glaciations during the Pleistocene (Hall, 2013) could have facilitated the vicariance of these populations, resulting in the fragmented present-day distribution on their respective land masses (Erik, 2003; Lim et al, 2017; Slik et al, 2011; Wurster et al, 2010). Within Peninsular Malaysia, the east-west pattern of lineage separation has been demonstrated in numerous co-distributed taxa (Chan, Abraham, Grismer, & Grismer, 2018; Chan et al, 2017, 2014; Grismer et al, 2013, 2015). The isolation of those taxa were hypothesized to be caused by the relatively central and contiguous Titiwangsa mountain range, which acts as an insurmountable physical barrier that separates habitats along the eastern and western regions (Chan et al, 2017; Chan & Brown, 2019).…”

“…Within Peninsular Malaysia, the east-west pattern of lineage separation has been demonstrated in numerous co-distributed taxa (Chan, Abraham, Grismer, & Grismer, 2018; Chan et al, 2017, 2014; Grismer et al, 2013, 2015). The isolation of those taxa were hypothesized to be caused by the relatively central and contiguous Titiwangsa mountain range, which acts as an insurmountable physical barrier that separates habitats along the eastern and western regions (Chan et al, 2017; Chan & Brown, 2019). We consider this proposed model to be incompatible with Pteroptyx , which occurs in mangroves and do not disperse across inland habitats to begin with.…”