Gene flow creates a mirage of cryptic species in a Southeast Asian
spotted stream frog complex
Abstract
Most new cryptic species are described using conventional tree- and
distance-based species delimitation methods (SDMs), which rely on
phylogenetic arrangements and measures of genetic divergence. However,
although numerous factors such as spatial population structure and gene
flow are known to confound phylogenetic and species delimitation
inferences, the influence of these processes on species estimation is
rarely evaluated. Using large amounts of exons, introns, and
ultraconserved elements obtained using the FrogCap sequence-capture
protocol, we compared conventional SDMs with more robust genomic
analyses that assesses spatial population structure and gene flow to
characterize species boundaries in a Southeast Asian frog complex
(Pulchrana picturata). Our results showed that gene flow and
introgression can produce phylogenetic patterns and levels of divergence
that resemble distinct species (up to 10% divergent in mitochondrial
DNA). Hybrid populations were inferred as independent (singleton) clades
that were highly divergent from adjacent populations (7–10%) and
unusually similar (<3%) to allopatric populations. Such
anomalous patterns are not uncommon in Southeast Asian amphibians, which
brings into question whether the high cryptic diversity observed in
other amphibian groups reflect distinct cryptic species—or, instead,
highly structured and admixed metapopulation lineages. Our results also
provide an alternative explanation to the conundrum of divergent
(sometimes non-sister) sympatric lineages―a pattern that has been
celebrated as indicative of true cryptic speciation. Based on these
findings, we recommend that species delimitation of continuously
distributed “cryptic” groups should not rely solely on conventional
SDMs but should necessarily examine spatial population structure and
gene flow to avoid taxonomic inflation.