Combining Phylogeography with Distribution Modeling: Multiple Pleistocene Range Expansions in a Parthenogenetic Gecko from the Australian Arid Zone

Abstract

Phylogenetic and geographic evidence suggest that many parthenogenetic organisms have evolved recently and have spread rapidly. These patterns play a critical role in our understanding of the relative merits of sexual versus asexual reproductive modes, yet their interpretation is often hampered by a lack of detail. Here we present a detailed phylogeographic study of a vertebrate parthenogen, the Australian gecko Heteronotia binoei, in combination with statistical and biophysical modeling of its distribution during the last glacial maximum. Parthenogenetic H. binoei occur in the Australian arid zone and have the widest range of any known vertebrate parthenogen. They are broadly sympatric with their sexual counterparts, from which they arose via hybridization. We have applied nested clade phylogeographic, effective migration, and mismatch distribution analyses to mitochondrial DNA (mtDNA) sequences obtained for 319 individuals sampled throughout the known geographic ranges of two parthenogenetic mitochondrial lineages. These analyses provide strong evidence for past range expansion events from west to east across the arid zone, and for continuing eastward range expansion. Parthenogen formation and range expansion events date to the late Pleistocene, with one lineage expanding from the northwest of its present range around 240,000 years ago and the second lineage expanding from the far west around 70,000 years ago. Statistical and biophysical distribution models support these inferences of recent range expansion, with suitable climatic conditions during the last glacial maximum most likely limited to parts of the arid zone north and west of much of the current ranges of these lineages. Combination of phylogeographic analyses and distribution modeling allowed considerably stronger inferences of the history of this complex than either would in isolation, illustrating the power of combining complementary analytical approaches.

Genetic and Genomic Interactions of Animals with Different Ploidy Levels

“…Genetic variation that is observed in some clones can often be tracked from extant bisexuals using cytogenetic, nuclear and mitochondrial markers. Multiple hybrid origins of polyploid asexual parthenogenetic lizards from diploid progenitors are well documented in the genus Aspidoscelis (formerly Cnemidophorus ) [Wright and Lowe, 1967;Neaves, 1971;Dessauer and Cole, 1989], Heteronotia binoei [Moritz 1984;Moritz et al, 1989;Strasburg et al, 2007] and in the genus Darevskia (formerly Lacerta ) [Moritz et al, 1992]. A hybrid origin for some parthenogenetic lizards is less clear or disputed.…”

“…The tetraploid females were viable and, through parthenogenesis, gave rise to tetraploid daughters and granddaughters. No diploid clones of H. binoei have been identified; the 2 major triploid clones (3N1 and 3N2) that arose from reciprocal hybridization of 2 bisexual populations of H. binoei have spread over much of Australia and are assumed to have independently arisen 240,000 (3N1) and 70,000 (3N2) years ago from possible diploid races [Strasburg et al, 2007]. Observed chromosomal variation within the triploid clones is attributed to past hybridization of bisexual individuals with the, presumably extinct, allodiploid races of H. binoei [Moritz et al, 1989;Strasburg et al, 2007].…”

“…No diploid clones of H. binoei have been identified; the 2 major triploid clones (3N1 and 3N2) that arose from reciprocal hybridization of 2 bisexual populations of H. binoei have spread over much of Australia and are assumed to have independently arisen 240,000 (3N1) and 70,000 (3N2) years ago from possible diploid races [Strasburg et al, 2007]. Observed chromosomal variation within the triploid clones is attributed to past hybridization of bisexual individuals with the, presumably extinct, allodiploid races of H. binoei [Moritz et al, 1989;Strasburg et al, 2007]. Although few meiotic data are available for the parthenogenetic lizards, Cuellar [1971] and Moritz [1984] speculated that meiosis in all of the parthenogenetic lizards involves a pre-meiotic endomitosis that is similar to meiosis in unisexual Ambystoma .…”

Coherent and incoherent inference in phylogeography and human evolution

“…Evolutionary history is written most clearly in such genomic regions, but other types of genetic data certainly do contain historic information and cannot be used by NCPA. Once hypotheses have been generated by coherent NCPA, coalescentsimulation approaches can be used for parameter estimation and for evaluating the compatibility of data sets other than haplotype trees with the hypotheses generated by NCPA (11). In this manner, NCPA and coalescent-simulation approaches should be regarded as complementary and synergistic approaches that both have a legitimate role in an integrated, phylogeographic inference scheme.…”

“…Alternative statistical approaches to phylogeography have been developed through coalescent simulations of specific phylogeographic models for both hypothesis testing and parameter estimation (9,10). NCPA and simulation approaches are not mutually exclusive, because both can be used in a synergistic fashion to produce deeper phylogeographic insight than possible with either approach alone (11). I show in this paper that some coalescent-simulation methods are incoherent and therefore have only limited utility in hypothesis testing but still can be used in a synergistic fashion with NCPA.…”