Asymmetric energetic costs in reciprocal-cross hybrids between carnivorous mice (Onychomys)

Abstract

Aerobic respiration is a fundamental physiological trait dependent on coordinated interactions between gene products of the mitochondrial and nuclear genomes. Mitonuclear mismatch in interspecific hybrids may contribute to reproductive isolation by inducing reduced viability (or even complete inviability) due to increased metabolic costs.However, few studies have tested for effects of mitonuclear mismatch on respiration at the whole-organism level. We explored how hybridization affects metabolic rate in closely related species of grasshopper mice (genus Onychomys) to better understand the role of metabolic costs in reproductive isolation. We measured metabolic rate across a range of temperatures to calculate basal metabolic rate (BMR) and cold-induced metabolic rate (MR c ) in O. leucogaster, O. torridus and O. arenicola, and in reciprocal F 1 hybrids between the latter two species. Within the genus, we found a negative correlation between mass-specific BMR and body mass. Although O. arenicola was smaller than O. torridus, hybrids from both directions of the cross resembled O. arenicola in body mass. In contrast, hybrid BMR was strongly influenced by the direction of the cross: reciprocal F 1 hybrids were different from each other but indistinguishable from the maternal species. In addition, MR c was not significantly different between hybrids and either parental species. These patterns indicate that metabolic costs are not increased in Onychomys F 1 hybrids and, while exposure of incompatibilities in F 2 hybrids cannot be ruled out, suggest that mitonuclear mismatch does not act as a primary barrier to gene flow. Maternal matching of BMR is suggestive of a strong effect of mitochondrial genotype on metabolism in hybrids. Together, our findings provide insight into the metabolic consequences of hybridization, a topic that is understudied in mammals.

Oxidative cost of interspecific hybridization: a case study of twoTriturusspecies and their hybrids

“…Phenotypically, hybrids can be similar to the paternal or maternal species due to dominance or the maternal effect, intermediate between the parental species, or it can exceed the qualities of both parental phenotypes (Wolf et al, 2010). Maternal matching was reported for basal metabolic rates of the grasshopper mouse hybrid (genus Onychomys), suggesting a strong effect of the mitochondrial genotype on the metabolism in hybrids (Shipley et al, 2016). Despite the fact that mitochondrial DNA is inherited from the maternal species and that mitochondria are the main source of ROS production, in this study we report that the hybrid has an AOS which is more similar to the paternal species (T. ivanbureschi).…”

Hybridization, sex-specific genomic architecture and local adaptation

“…Cytonuclear incompatibilities arising from hybridization between diverged taxa are found in a range of taxa, e.g. in birds [63][64][65], carnivorous mice [66], flat worms [67] and plants [68,69]. Suboptimal respiration is one of the fitness costs to hybrids in flycatchers [64], carnivorous mice [66], voles [70] and chickadees [71], likely due to mitonuclear incompatibilities.…”

“…in birds [63][64][65], carnivorous mice [66], flat worms [67] and plants [68,69]. Suboptimal respiration is one of the fitness costs to hybrids in flycatchers [64], carnivorous mice [66], voles [70] and chickadees [71], likely due to mitonuclear incompatibilities. Mitonuclear incompatibilities have also been shown to distort sex ratios, e.g.…”

Hybridization, sex specific genomic architecture and local adaptation

“…on ageing [52,54] [60,61]. Suboptimal respiration is one of the fitness costs to hybrids in flycatchers [56], carnivorous mice [58], voles [62], and chickadees [63], likely due to mito-nuclear incompatibilities. The findings of heteroplasmy in hybrids across a wide range of taxa, including mussels [64], wheat [65], birds [55,57] and Drosophila [66] could potentially be due to selection for paternal leakage to counteract negative fitness effects of matrilinearily inherited mitochondria [67].…”