Gene duplicates resolving sexual conflict rapidly evolved essential gametogenesis functions

VanKuren, Nicholas W.; Long, Manyuan

doi:10.1038/s41559-018-0471-0

Cited by 73 publications

(97 citation statements)

References 54 publications

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“…First, loci under IASC may undergo duplication, which allows for different paralogs to become expressed in males and females (Connallon & Clark, 2011;Ellegren & Parsch, 2007;Parsch & Ellegren, 2013). Following this, they may acquire a sex-limited role, as was recently found for the gene duplicates Artemis (Arts) and Apollo (Apl) in D. melanogaster (VanKuren & Long, 2018), which are involved in respectively egg elongation and spermatid individualization. Arts and Apl arose by duplication some 200,000 years ago, followed by Arts becoming predominantly expressed in females, whereas Apl became active mostly in males.…”

Section: Separating the Genetic Architectures Of Male And Female Fimentioning

confidence: 99%

Making sense of intralocus and interlocus sexual conflict

Schenkel

Pen

Beukeboom

et al. 2018

Ecology and Evolution

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Sexual conflict occurs because males and females are exposed to different selection pressures. This can affect many aspects of female and male biology, such as physiology, behavior, genetics, and even population ecology. Its broad impact has caused widespread interest in sexual conflict. However, a key aspect of sexual conflict is often confused; it comprises two distinct forms: intralocus and interlocus sexual conflict (IASC and IRSC). Although both are caused by sex differences in selection, they operate via different proximate and ultimate mechanisms. Intralocus sexual conflict and IRSC are often not clearly defined as separate processes in the scientific literature, which impedes a proper understanding of each form as well as of their relative impact on sexual conflict. Furthermore, our current knowledge of the genetics of these phenomena is severely limited. This prevents us from empirically testing numerous theories regarding the role of these two forms of sexual conflict in evolution. Here, we clarify the distinction between IASC and IRSC, by discussing how male and female interests differ, how and when sex‐specific adaptation occurs, and how this may lead to evolutionary change. We then describe a framework for their study, focusing on how future experiments may help identify the genetics underlying these phenomena. Through this, we hope to promote a more critical reflection on IASC and IRSC as well as underline the necessity of genetic and mechanistic studies of these two phenomena.

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Section: Separating the Genetic Architectures Of Male And Female Fimentioning

confidence: 99%

Making sense of intralocus and interlocus sexual conflict

Schenkel

Pen

Beukeboom

et al. 2018

Ecology and Evolution

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“…It is possible that relocated genes (and duplicated genes) could have experienced strong positive or purifying selection immediately after duplication (or loss of the ancestral paralog), and the signatures of those selection pressures were lost over time. Analysis of a large panel of young duplications and relocations are necessary to test this hypothesis (e.g., Masly et al, 2006;VanKuren and Long, 2018). However, our observation that the D. melanogaster orthologs of D. pseudoobscura relocated genes also evolve under relaxed constraints ( Supplementary Fig S1) suggests that relocated genes have evolved under relaxed constraints for most of their histories.…”

Section: Discussionmentioning

confidence: 97%

“…In addition, the derived copies of dispersed duplicates tend to experience positive selection or relaxed constraints (Kondrashov et al, 2002;Conant and Wagner, 2003;Han et al, 2009;Han and Hahn, 2012), while mammalian relocated genes appear to evolve under strong purifying selection (Ciomborowska et al, 2013). It has been hypothesized that positive selection on the derived copies of duplicated genes fixes mutations that improve testis-specific functions once pleiotropic constraints are relaxed by duplication (Betrán and Long, 2003;Torgerson and Singh, 2004;Betrán et al, 2006;Rosso et al, 2008;Meisel et al, 2010;Quezada-Diaz et al, 2010;Tracy et al, 2010;VanKuren and Long, 2018). Gene relocation is unlikely to resolve pleiotropic conflicts because a second copy of the gene is not retained.…”

Section: Introductionmentioning

confidence: 99%

Genes relocated betweenDrosophila chromosomearms evolve under relaxed selective constraints relative to non-relocated genes

Hart

Bolden

et al. 2017

Preprint

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Gene duplication creates a second copy of a gene either in tandem to the ancestral locus or dispersed to another chromosomal location. When the ancestral copy of a dispersed duplicate is lost from the genome, it creates the appearance that the gene was "relocated" from the ancestral locus to the derived location. Gene relocation may be as common as canonical dispersed duplications in which both the ancestral and derived copies are retained, but relocated genes have received far less attention than canonical duplicates. To test this hypothesis, we combined comparative genomics, population genetics, gene expression, and functional analyses to assess the selection pressures acting on relocated, duplicated, and nonrelocated single-copy genes in Drosophila genomes. We find that relocated genes evolve faster than single-copy non-relocated genes, and there is no evidence that this faster evolution is driven by positive selection. In addition, relocated genes are less essential for viability and male fertility than single-copy non-relocated genes, suggesting that relocated genes evolve fast because of relaxed selective constraints. The derived copies of canonical dispersed duplicated genes evolve even faster than relocated genes, and there is no evidence that this faster evolution is driven by positive selection. The derived copies of dispersed duplicates are also more narrowly expressed than relocated genes, which suggests that the evolution of canonical duplicates is less selectively constrained than relocated genes. We therefore conclude that relocated genes are under more selective constraints than canonical duplicates, but are not as conserved as single-copy non-relocated genes.

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“…Under such circumstances, it is expected that this impasse should be resolved by transcriptional rewiring, which can occur rapidly. For example, Apollo and Artemis nuclear importin genes duplicated and transcriptionally diverged ~200,000 years ago in the D. melanogaster lineage 69 . While Apollo is required for male fertility, it is detrimental to female fertility, while the opposite is true for Artemis 69 .…”

Section: Discussionmentioning

confidence: 99%

“…For example, Apollo and Artemis nuclear importin genes duplicated and transcriptionally diverged ~200,000 years ago in the D. melanogaster lineage 69 . While Apollo is required for male fertility, it is detrimental to female fertility, while the opposite is true for Artemis 69 . By analogy, we would predict that males should lose Arp53D expression in testes to relieve male fertility defects but maintain female and zygotic expression.…”

Section: Discussionmentioning

confidence: 99%

A rapidly evolving actin mediates fertility and developmental tradeoffs inDrosophila

Schroeder

Tomlin

Valenzuela

et al. 2020

Preprint

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Most actin-related proteins (Arps) are highly conserved in eukaryotes, where they carry out well-defined cellular functions. Drosophila and mammals also encode divergent non-canonical Arps in their male-germline whose roles remain unknown. Here, we show that Arp53D, a rapidly-evolving Drosophila Arp, localizes to fusomes and actin cones, two male germline-specific actin structures critical for sperm maturation, via its non-canonical N-terminal tail. Although we expected that Arp53D loss would reduce male fertility, we instead find that Arp53D-KO males are more fertile, both in isolation and in competition with wildtype males. Upon investigating why evolution would retain a gene that negatively impacts male fertility, we unexpectedly found that Arp53D-KO females are less fertile. Moreover, KO embryos exhibit reduced viability, which worsens under heat stress. We conclude that ‘testis-specific’ Arp53D is detrimental to male fertility, but is required for female fertility and early development, leading to its long-term retention and recurrent adaptation in Drosophila.

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Gene duplicates resolving sexual conflict rapidly evolved essential gametogenesis functions

Cited by 73 publications

References 54 publications

Making sense of intralocus and interlocus sexual conflict

Making sense of intralocus and interlocus sexual conflict

Genes relocated betweenDrosophila chromosomearms evolve under relaxed selective constraints relative to non-relocated genes

A rapidly evolving actin mediates fertility and developmental tradeoffs inDrosophila

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