Acquisition of Germ Plasm Accelerates Vertebrate Evolution

Evans, Teri; Wade, Christopher M.; Chapman, Frank A.; Johnson, Andrew D.; Loose, Matthew

doi:10.1126/science.1249325

Cited by 50 publications

(94 citation statements)

References 75 publications

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“…Or, the quantification may be associated with rate of speciation. For example, for sequences evolving at significantly different rates, 87% of the sequences show anurans evolving faster than caudates [24].…”

Section: Resultsmentioning

confidence: 99%

“…One empirical system in which evolvability has been invoked to explain species richness asymmetry in sister clades and differential rates of speciation, has been primordial germ cell (PGC) determination mechanisms [21][22][23][24]. Primordial germ cells are the precursor cells that eventually form eggs and sperm in the developing embryo.…”

Section: A Biological Example Of Evolvability: Primordial Germ Cell Dmentioning

confidence: 99%

“…An observation of equal importance by Evans et al is "No other biological property correlates as well with the observed changes in rate. " The biological property they refer to is the determinative mechanism (through the proxy of the presence of germ plasm) [24].…”

Section: A Biological Example Of Evolvability: Primordial Germ Cell Dmentioning

confidence: 99%

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Linking a Biological Mechanism to Evolvability

Crother¹,

Murray²

2018

J Phylogenetics Evol Biol

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Evolvability has become a concept used to explain the common observation of clade asymmetry. However, the concept of evolvability means different things to different workers. Recent work has formalized the concept and we apply the formalized concept to a developmental system (primordial germ cell determination mechanism) that has been proposed to explain clade size disparity. In a simplified view, there are two general primordial germ cell (pgc) determination mechanisms: determinative and induced. The determinative mechanism is associated with species rich clades and the induced mechanism with species poor clades. The formal equations of evolvability provide a theoretical framework under which we can assess the relative influence of pgc determination mechanisms on clade evolvability. We propose that the determinative mechanism has enhanced evolvability in most clades that possess the trait.

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Section: Resultsmentioning

confidence: 99%

Section: A Biological Example Of Evolvability: Primordial Germ Cell Dmentioning

confidence: 99%

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Linking a Biological Mechanism to Evolvability

Crother¹,

Murray²

2018

J Phylogenetics Evol Biol

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“…The hypothesis' predictions pertaining to molecular evolution of genes has been purported to be empirically supported by findings of faster evolution of protein sequences in clades with inheritance than in clades with induction (faster rates were inferred for up to 32% of the genes in a genome under inheritance) based on analysis of four pairs of vertebrates, with one member of the pair exhibiting inheritance and the other induction [anurans vs. urodeles, birds vs. crocodiles/turtles, snakes vs. lizards, and one clade of ray-finned fishes (Teleostei) vs. another (Acipenseriformes) (20)]. As with any hypothesis, testing the predictions by using different methods and systems would be helpful to assessing its generalizability, particularly because that pioneering assessment had some limitations.…”

Section: Evaluation Of the Pgc-specification Hypothesismentioning

confidence: 99%

“…Small gene sample sizes for some taxa, the use of tissue-specific transcriptomes, and exclusion of invertebrates, which comprise the vast majority of animal life, also may have limited those findings (25) (see further details on these limitations in SI Appendix, section 2). Accordingly, further investigations using alternate approaches and organisms would be useful to assess whether the purported liberation of constraint and increase in rates of protein-coding sequence evolution under germ plasm (20) is robust to different types of methods and animal systems.…”

Section: Evaluation Of the Pgc-specification Hypothesismentioning

confidence: 99%

Causes and evolutionary consequences of primordial germ-cell specification mode in metazoans

Whittle

Extavour

2017

Proc. Natl. Acad. Sci. U.S.A.

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In animals, primordial germ cells (PGCs) give rise to the germ lines, the cell lineages that produce sperm and eggs. PGCs form in embryogenesis, typically by one of two modes: a likely ancestral mode wherein germ cells are induced during embryogenesis by cell-cell signaling (induction) or a derived mechanism whereby germ cells are specified by using germ plasm-that is, maternally specified germ-line determinants (inheritance). The causes of the shift to germ plasm for PGC specification in some animal clades remain largely unknown, but its repeated convergent evolution raises the question of whether it may result from or confer an innate selective advantage. It has been hypothesized that the acquisition of germ plasm confers enhanced evolvability, resulting from the release of selective constraint on somatic gene networks in embryogenesis, thus leading to acceleration of an organism's protein-sequence evolution, particularly for genes expressed at early developmental stages, and resulting in high speciation rates in germ plasm-containing lineages (denoted herein as the "PGCspecification hypothesis"). Although that hypothesis, if supported, could have major implications for animal evolution, our recent large-scale coding-sequence analyses from vertebrates and invertebrates provided important examples of genera that do not support the hypothesis of liberated constraint under germ plasm. Here, we consider reasons why germ plasm might be neither a direct target of selection nor causally linked to accelerated animal evolution. We explore alternate scenarios that could explain the repeated evolution of germ plasm and propose potential consequences of the inheritance and induction modes to animal evolutionary biology.germ line | preformation | epigenesis | primordial germ cell | spandrel P rimordial germ cells (PGCs) are specialized cells located in sexual organs of animals. These cells are central to reproduction because they give rise to the germ lines and, ultimately, the sperm and eggs. The PGCs typically arise during early embryogenesis by one of two distinct modes: (i) induction, wherein germ cells are induced by cell-cell signaling pathways (also known as epigenesis); or (ii) inheritance, wherein germ cells are formed by using germ plasm (a specialized cytoplasm containing proteins and RNAs needed for PGC formation), that is, maternally generated germ-line determinants that are "preformed" before embryogenesis begins (also known as preformation) (1-3). The induction mode appears to be the more prevalent mode in animals and occurs in basally branching lineages, and thus is the hypothesized ancestral mechanism of PGC specification, whereas inheritance comprises the likely derived state (1) (Fig. 1) (see SI Appendix, section 1 on the less parsimonious scenario that induction is the derived mode). Induction has been inferred based on microscopic data from most animal clades studied to date and has been experimentally shown to occur in a diverse range of organisms, including mammals (Mus musculus) (4-8), salamanders (...

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Germ-Cell Formation in Solitary Ascidians: Coexistence of Preformation and Epigenesis

Shirae-Kurabayashi

Nakamura

2018

Diversity and Commonality in Animals

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Acquisition of Germ Plasm Accelerates Vertebrate Evolution

Cited by 50 publications

References 75 publications

Linking a Biological Mechanism to Evolvability

Linking a Biological Mechanism to Evolvability

Causes and evolutionary consequences of primordial germ-cell specification mode in metazoans

Germ-Cell Formation in Solitary Ascidians: Coexistence of Preformation and Epigenesis

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