Phenotypic Variation in Mitochondria-Related Performance Traits Across New Zealand Snail Populations

Abstract

Mitochondrial function is critical for energy homeostasis and should shape how genetic variation in metabolism is transmitted through levels of biological organization to generate stability in organismal performance. Mitochondrial function is encoded by genes in two distinct and separately inherited genomes - the mitochondrial genome and the nuclear genome - and selection is expected to maintain functional mito-nuclear interactions. The documented high levels of polymorphism in genes involved in these mito-nuclear interactions and wide variation for mitochondrial function demands an explanation for how and why variability in such a fundamental trait is maintained. Potamopyrgus antipodarum is a New Zealand freshwater snail with coexisting sexual and asexual individuals and, accordingly, contrasting systems of separate vs. co-inheritance of nuclear and mitochondrial genomes. As such, this snail provides a powerful means to dissect the evolutionary and functional consequences of mito-nuclear variation. The lakes inhabited by P. antipodarum span wide environmental gradients, with substantial across-lake genetic structure and mito-nuclear discordance. This situation allows us to use comparisons across reproductive modes and lakes to partition variation in cellular respiration across genetic and environmental axes. Here, we integrated cellular, physiological, and behavioral approaches to quantify variation in mitochondrial function across a diverse set of wild P. antipodarum lineages. We found extensive across-lake variation in organismal oxygen consumption and behavioral response to heat stress and differences across sexes in mitochondrial membrane potential but few global effects of reproductive mode. Taken together, our data set the stage for applying this important model system for sexual reproduction and polyploidy to dissecting the complex relationships between mito-nuclear variation, performance, plasticity, and fitness in natural populations.

Single-molecule Sequencing of an Animal Mitochondrial Genome Reveals Chloroplast-like Architecture and Repeat-mediated Recombination

“…These native New Zealand prosobranch snails are well-studied because of the status of P. antipodarum as a model system for sexual reproduction, host–parasite coevolution, and as a worldwide invader. Interest in how the consequences of reproductive mode polymorphism might influence mitochondrial evolution and the maintenance of sex has motivated surveys revealing extensive genetic variation in mtDNA ( Neiman and Lively 2004 ; Neiman et al 2010 ; Paczesniak et al 2013 ; Sharbrough et al 2018 ) as well as a phenotypic variation for mitochondrial function ( Sharbrough et al 2017 ; Greimann et al 2020 ) in P. antipodarum . Although previous efforts to sequence P. antipodarum mitochondrial genomes have provided valuable data on this front ( Neiman et al 2010 ; Sharbrough et al 2018 ), all have been restricted to short sequencing reads or PCR-amplified segments, and none have been able to assemble the entire circular structure.…”

“…The New Zealand freshwater snail Potamopyrgus antipodarum ( fig. 1 ) is a powerful model for a number of ecological and evolutionary questions, including the maintenance of sex ( Lively 1987 ), consequences of polyploidy ( Neiman et al 2011 ), host–parasite dynamics ( Jokela and Lively 1995 ; Gibson et al 2016 ; Bankers et al 2017 ), biology of invasive organisms ( Levri and Clark 2015 ), and mitonuclear coevolution ( Neiman et al 2010 ; Paczesniak et al 2013 ; Sharbrough et al 2017 , 2018 ; Greimann et al 2020 ). To generate the whole-genome resources needed to investigate these fundamental topics, we used a combination of Illumina HiSeq (DNA and RNA), MiSeq, and PacBio long-read technologies to sequence total cellular DNA from an inbred (∼25 generations) sexual lineage of P. antipodarum and wild-caught specimens of its close relative ( Haase 2008 , our data), P. estuarinus .…”

A tale of two genomes: What drives mitonuclear discordance in asexual lineages of a freshwater snail?

“…The data needed to evaluate these predictions do not exist. We do know that Potamopyrgus mitochondrial genomes exhibit signs of inter‐haplotype recombination and apparent heteroplasmy [ 78 ] and signatures of sex‐specific optima of mitochondrial function [ 79 ] , indicating that this type of sexual conflict is at least biologically possible in P. antipodarum . Additional tests of inheritance patterns in sexual lineages will provide a critical test of whether “leaky” mitochondrial inheritance exists in this species.…”

Single-molecule sequencing of animal mitochondrial genomes reveals chloroplast-like architecture and repeat-mediated recombination

“…The New Zealand freshwater snail, Potamopyrgus antipodarum (Figure 1), is a powerful model for a number of ecological and evolutionary questions, including the maintenance of sex (42), consequences of polyploidy (43), host-parasite dynamics (44–46), biology of invasive organisms (47), and mitonuclear coevolution (25, 28, 48, 49). To generate the whole-genome resources needed to investigate these fundamental topics, we used a combination of Illumina HiSeq (DNA and RNA), MiSeq, and PacBio long-read technologies to sequence total cellular DNA from an inbred (∼25 generations) sexual lineage of P. antipodarum and wild-caught specimens of its close relative ((50), our data), P. estuarinus .…”