Cytonuclear genomic dissociation in African elephant species

Abstract

African forest and savanna elephants are distinct species separated by a hybrid zone. Because hybridization can affect the systematic and conservation status of populations, we examined gene flow between forest and savanna elephants at 21 African locations. We detected cytonuclear dissociation, indicative of different evolutionary histories for nuclear and mitochondrial genomes. Both paternally (n = 205 males) and biparentally (n = 2,123 X-chromosome segments) inherited gene sequences indicated that there was deep genetic separation between forest and savanna elephants. Yet in some savanna locales distant from present-day forest habitats, many individuals with savanna-specific nuclear genotypes carried maternally transmitted forest elephant mitochondrial DNA. This extreme cytonuclear dissociation implies that there were ancient episodes of hybridization between forest females and savanna males, which are larger and reproductively dominant to forest or hybrid males. Recurrent backcrossing of female hybrids to savanna bulls replaced the forest nuclear genome. The persistence of residual forest elephant mitochondria in savanna elephant herds renders evolutionary interpretations based on mitochondrial DNA alone misleading and preserves a genomic record of ancient habitat changes.

Extensive mitochondrial introgression in North American Great Black-backed Gulls (Larus marinus) from the American Herring Gull (Larus smithsonianus) with little nuclear DNA impact

“…Similar mito-nuclear discordances in the amount of introgression has been documented for a wide range of animal species, in some cases leading to the complete replacement of the mtDNA of the introgressed species by the mtDNA of the other species without any evidence of nuclear introgression (reviewed in Toews and Brelsford, 2012). The pattern we uncovered in North American MARINUS is, for example, similar to the savanna elephant (Loxodonta africana) where mtDNA from the closely related forest elephant (L. cyclotis) reached a high frequency, but none of the three biparentally inherited loci contained any foreign alleles (Roca et al, 2005). Several hypotheses have been proposed to explain such mitonuclear discrepancies in levels of introgression in vertebrates; they can broadly be divided between selective and neutral (demographic) processes (listed in Hedrick, 2010).…”

“…Selective hypotheses propose stronger selection against alien nuclear alleles than mitochondrial haplotypes (Funk and Omland, 2003) and positive selection on introgressed mtDNA variants. We will examine these different hypotheses below.Unidirectional mating and subsequent backcrossing has been invoked to explain some striking instances of discordant mito-nuclear introgression (for example, Roca et al, 2005, see also Hedrick, 2010. As rightly noted by these authors, hybridization of a species A female with a species B male and subsequent backcrossing of female progeny with species B males produce individuals with species A mtDNA but with essentially species B nuclear background, because the ancestry of species A in the nuclear genome halves at each generation of backcrossing.…”

Phylogenomic evidence for ancient hybridization in the genomes of living cats (Felidae)

“…In addition, felid inter-species hybrids follow Haldane's Rule (Haldane 1922) specifically as it relates to hybrid sterility: Females are generally fertile, while males are overwhelmingly sterile (Gray 1972;Davis et al 2015). Unisexual sterility coupled with male-biased dispersal promotes situations where the mitochondrion of one species or lineage may persist within the genomic background of a different species following introgression into one of the parental populations (e.g., Roca et al 2005). This pattern is exemplified by the northeastern tigrina and the fishing cat genomes, which possess mitochondrial DNA more similar to that of a different species.…”

“…There is an emerging consensus that gene flow frequently occurs following speciation despite the establishment of reproductive barriers that otherwise maintain species-level distinctiveness (Roca et al 2005;Good et al 2008;Ellegren et al 2012;Garrigan et al 2012;Toews and Brelsford 2012;Cahill et al 2013Cahill et al , 2014Cui et al 2013;Martin et al 2013;Kutschera et al 2014;Sullivan et al 2014). However, incomplete lineage sorting (ILS) is assumed by default to underpin most cases of phylogenetic discordance.…”

“…However, incomplete lineage sorting (ILS) is assumed by default to underpin most cases of phylogenetic discordance. Few studies in the literature account for hybridization by analyzing all inheritance patterns (uniparental, sex-biased, biparental) with high-resolution data, or instead have focused on only a few species (Roca et al 2005;Cahill et al 2013Cahill et al , 2014Trigo et al 2013;Khan et al 2014). The cat family Felidae contains 38 recognized species within eight lineages (designated henceforth by a capitalized name, e.g., Puma lineage) that vary in the breadth of their geographic occurrence (Buckley-Beason et al 2006;Johnson et al 2006).…”