Phylogenetic evidence of mitochondrial DNA introgression among pocket gophers in New Mexico (family Geomyidae)

Abstract

Mitochondrial DNA (mtDNA) variation in the cytochrome b gene was determined for two divergent taxa of pocket gophers, Thomomys bottae actuosus and T. b. ruidosae. These two taxa hybridize in a narrow contact zone, but introgression of nuclear markers such as allozymes or chromosomes does not extend much beyond the hybrid zone (Patton et al. 1979). We found that despite their distinctness, the two subspecies shared very similar mtDNA haplotypes. By a comparison of phylogenetic histories derived from nuclear markers (allozymes) and from mtDNA haplotypes sampled in different populations of T. bottae from New Mexico, we show that apparent similarity is due to an introgression of T. b. ruidosae mtDNA into T. b. actuosus nuclear background. Evidence of introgression is not limited to the present-day contact zone between these two taxa, but extends at least 75 km away from it. The actuosus haplotype coexists along with the ruidosae mtDNA in the Gallinas Mts., which are inhabited by otherwise pure T. b. actuosus, while further north only typical actuosus haplotypes were detected. Of several potential mechanisms which could lead to such a geographical pattern of variation, we argue that a combination of range shifts due to climatic fluctuations, and genetic drift are most likely. Horizontal gene transfers due to hybridization are historical events which seem rather common among pocket gophers. Although they can be identified with careful phylogenetic study using independent data sets, the potential for misinterpreting a gene tree as an organismal tree is great in this and other groups of animals.

Empirical study of hybrid zone movement

“…In a further 13 hybrid zones, patterns of introgression might be interpreted as evidence for movement: gulls Larus glaucescens and Larus occidentalis (Bell, 1996;Gay, 2006); pocket gophers Thomomys townsendii and Thomomys bottae (Patton, 1993;Patton and Smith, 1993); Thomomys bottae actuosus and Thomomys bottae ruidosae (Ruedi et al, 1997); fish Gambusia affinis and Gambusia holbrooki (Reznick, 1981;Scribner, 1993;Scribner and Avise, 1993;Scribner and Avise, 1994a, b); hares Lepus granatensis/Lepus europaeus and Lepus timidus (Thulin and Tegelströ m, 2002;Melo-Ferreira et al, 2005, 2007; salamander Chioglossa lusitanica North and South forms (Sequeira et al, 2005); mussels Mytilus galloprovincialis and Mytilus edulis (Gardner and Skibinski, 1988;Skibinski and Roderick, 1991;Willis and Skibinski, 1992;Gardner et al, 1993;Wilhelm and Hilbish, 1998;Bierne et al, 2003); beetles Carabus albrechti and Carabus lewisianus (Takami and Suzuki, 2005); lizard Sceloporus grammicus chromosomal races F5 and FM2 (Sites et al, 1996;Marshall and Sites, 2001) cottonwoods Populus angustifolia and Populus fremontii (Keim et al, 1989;Paige et al, 1991;Martinsen et al, 2001).…”

“…Increased rainfall may have favoured tick species A. hydrosauri at a hybrid zone with A. limbatum (Bull and Burzacott, 2001) and climate fluctuations may have caused movement in a T. b. actuosus-T. b. ruidosae hybrid zone (Ruedi et al, 1997). Human-induced climate change appears to have caused movement of the Pholidobolus montium-Pholidobolus affinis (lizards) hybrid zone, when fields which had been rocky with numerous agaves were cleared of rocks, irrigated and planted with crops (Hillis and Simmons, 1986), and hybridization between salamanders P. jordani and P. glutinosus may have increased due to intense timbering (Hairston et al, 1992).…”

“…fasciatus hybrid zone in the recent past (Britch et al, 2001). Past movements evidenced by introgression patterns in the L. granatensis-L. europaeus (Melo-Ferreira et al, 2007), T. b. actuosus-T. b. ruidosae (Ruedi et al, 1997) and Caledia captiva (Shaw et al, 1993) hybrid zones have been attributed to Pleistocene climate changes. This suggests that hybrid zone movements could provide biological indicators of climate change, an application that could be of public interest in coming years.…”

Pliocene and Pleistocene diversification and multiple refugia in a Eurasian shrew (Crocidura suaveolens group)

“…The congruence between genetic data and classical morphological interpretations was then examined. Considering that the mitochondrial genome of a taxon can introgress into another closely related taxon (Arntzen and Wallis, 1991;Ruedi et al, 1997;Tegelstrom, 1987), a fragment of the nuclear gene Breast Cancer Susceptibility 1 (BRCA1) was analysed in certain samples. Using such data from both mitochondrial and nuclear genomes, and considering the molecular clock, the colonisation and diVerentiation of the populations through time and space was reconstructed.…”

African Mole-rats (Bathyergidae): A Complex Radiation in Tropical Soils

“…In this chapter it is our intention to review what is known about the phylogenetic relationships in Bathyergidae, with particular emphasis on the central African clade (Cryptomys/Fukomys) and present the evidence that shows how taxonomic differentiation has been influenced by past climatic and geomorphological factors. We realise that factors other than the historical geographic setting affect evolution in these subterranean rodents, including evolutionary constraints set by population demography on reproductive isolating mechanisms and enhancement of divergence through hybridisation (Golding and Strobeck 1983;Harrison 1993;Ruedi et al 1997;Grant and Grant 1997;Steinberg and Patton 2000). At this stage, however, demographic studies and the role of hybridisation as an evolutionary mechanism have not received explicit attention in bathyergids.…”