Introgression of mitochondrial DNA promoted by natural selection in the Japanese pipistrelle bat (Pipistrellus abramus)

Abstract

Introgression of mitochondrial DNA (mtDNA) between closely related taxa can be promoted by either neutral processes or natural selection. Since mitochondrial gene-encoded proteins play critical roles in oxidative metabolism, mtDNA genes are commonly considered to experience strong selective constraint. However, metabolic requirements vary across climatic and ecological gradients, thus modifying potential selective pressures acting on mtDNA genes. Here we conducted tests to detect adaptive evolution occurring in two mtDNA genes (Cytb and ND5) in individuals of Japanese pipistrelle bat (Pipistrellus abramus) across the mainland of China and Hainan Island. Nuclear DNA markers identified two clades in both the mainland and Hainan Island populations, whereas each of these regions had a specific mtDNA clade. This cyto-nuclear discordance is most likely caused by introgression of the mtDNA by ruling out two other alternative scenarios (incomplete lineage sorting and sex-biased gene flow). Although population-based analyses revealed purifying selection acting on Cytb and neutrality in ND5, multiple nonsynonymous substitutions in both Cytb and ND5 were suggested to have been caused by positive selection by a divergence-based analysis. Our study supports the view that molecular adaptation can occur at genes under strong purifying selection if nonsynonymous substitutions cause radical changes in the physicochemical properties of amino acids.

Strong Amerindian Mitonuclear Discordance in Puerto Rican Genomes Suggests Amerindian Mitochondrial Benefit

“…While there is some evidence of positive selection of mitochondrial polymorphisms in bats (Dong et al., ), hare (Melo‐Ferreira et al., ), and vole (Boratynski et al. ), leading to mitonuclear discordance, specific adaptive benefits of mitochondrial polymorphisms have been difficult to assign (Melo‐Ferreira et al., ), Likewise, while there is some evidence of population‐specific adaptation in human mitochondrial genomes (Mishmar et al., ; Ruiz‐Pesini et al., ; Kivisild et al., , although see Elson et al., ; Ingman and Gyllensten, ), identifying adaptive benefits with specific polymorphisms has been difficult.…”

“…Here, I use the term to refer to gene flow between species, while I describe the analogous process within species that leads to mitonuclear discordance as “disproportionate mitochondrial expansion.” Within mammals, mitochondrial introgression is common and has been shown to occur in at least 25 species (Toew & Brelsford, ). Within species, disproportionate mitochondrial expansion has been observed within a species of bat (Dong et al., ) and a species of mouse (Spiridonova, 2014). In the case of humans, there is no evidence of mitochondrial introgression between species.…”

Evidencia de introgresión genética entre Pteronotus fulvus y Pteronotus gymnonotus (Chiroptera: Mormoopidae)

“…La dirección y el grado de introgresión genética, así como las consecuencias evolutivas, presentan una dinámica muy variable debido a que dependen de una variedad de factores tales como el grado de solapamiento de la distribución de las especies parentales, la compatibilidad del genoma, las estrategias de apareamiento, la dispersión, los patrones en su estructura social y las presiones selectivas (Arnold, 1992;Mao et al 2010). Una forma común de detectar la introgresión es mediante la discordancia en los análisis filogenéticos a partir de ADN mitocondrial (ADNmt) y el ADN nuclear (ADNnc) (Dong et al 2014). Sin embargo, la discordancia filogenética también puede ser resultado de la clasificación incompleta de linajes por polimorfismo ancestral (Ballard y Whitlock, 2004;.…”

“…Este fenómeno es frecuentemente asociado con una expansión demográfica abrupta del taxón invasor (Currat et al 2008;Petit y Excoffier, 2009;Mao et al 2012). Este modelo ha sido observado en varias especies de murciélagos, donde el ADNmt de la población colonizadora ha sido reemplazado por el de la población residente Dong et al 2014;Kuo et al 2015).…”

“…Debido a la importancia de las proteínas codificadas por el ADNmt en la fosforilación oxidativa del ADNmt, la selección purificadora ha sido considerada como la fuerza dominante en su historia evolutiva, no obstante existen estudios que han proporcionado evidencia de selección adaptiva en los genes mitocondriales de los mamíferos (Stewart et al 2008;, también encontrada en murciélagos (Dong et al 2014) y se sabe que el metabolismo mitocondrial es altamente sensible a las condiciones ambientales, especialmente a la variación de la temperatura (Dong et al 2014).…”