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Mutation-Driven Evolution: Microsatellite Instability Drives Speciation in a Mammalian Taxon

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Book cover Evolutionary Biology: Biodiversification from Genotype to Phenotype

Abstract

The concept of evolvability —from its evolutionary origins to molecular mechanisms—defines a fundamental problem at the intersection of biochemistry, genetics, and developmental biology. An emerging paradigm, mutation-driven evolution, posits that chromosomal dynamics (including changes in ploidy, chromosome loss, aberrant recombination, and mechanics of DNA damage and repair) underlie the origin of genetic variation as a precondition for selection. A model is provided by microsatellite instability. Although widely exploited as an experimental marker of evolutionary change with application to human disease, the potential contribution of such instability to evolvability itself is less well understood. Here, we propose that microsatellite instability within a vertebrate sex-determining gene can drive rapid adaptation and speciation. Our analysis focuses on superfamily Muroidea (order Rodentia) wherein four anomalies are observed: (1) This superfamily is unusually speciose, indeed the most species rich in Mammalia; (2) speciation has occurred rapidly (i.e., within the past 25 million years) and apparently in overlapping ranges; (3) inherited XY sex reversal has evolved independently within multiple genera; and (4) uniquely among therian mammals, male sex-determining mechanisms not dependent on Y-encoded testis-determining factor Sry have emerged. A unifying hypothesis is presented whereby these anomalies have a single molecular basis, to wit the dynamics of a Muroidea-specific microsatellite-encoded transcriptional activation domain. An ancestral microsatellite in this taxon has functioned as a “genetic capacitor ” to enable cryptic variation to accumulate within Sry. On discharge, this capacitor provided a recurring source of reproductive isolation and thus enabled rapid evolution of biological novelty at the edge of sexual ambiguity.

Amino acids are designated by standard three-letter code.

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Notes

  1. 1.

    SOX9 also functions in the specification of cartilage and morphogenesis of bone, and so its mutation gives rise to the syndrome of campomelic dysplasia (Foster et al. 1994). Related phenotypes occur in association with deletion of upstream regulatory elements in the SOX9 gene (Sekido and Lovell-Badge 2008).

  2. 2.

    Proof of principle was provided in studies of chimeric mouse Sry genes containing the human SRY HMG box (Chen et al. 2013b). In this chimera the mouse GRD compensates for a human clinical mutation associated with partial loss of specific DNA-binding activity.

  3. 3.

    Since submission of this chapter, a study by Montes et al has suggested an earlier date for the formation of the Panamanian land bridge. Based on uranium-lead dating of sedimentary-river deposits in the Andes, the authors have concluded that the Isthmus of Panama existed in the middle Miocene, approximately 15 million years ago (Montes et al. 2015). This revised geological estimate promises in part to explain the broad radiation of Muroid rodents in South America.

  4. 4.

    Infertility may ordinarily arise in such cases due to antagonistic effects of other Y-chromosome linked genes. Indeed, the presence of Y-linked gene Zfy2 (near Sry on the short arm) was recently found to cause loss of fertility in outbred (Sry -) sex-reversed XY female mice as its deletion partially restored fertility (Vernet et al. 2014). Analogous incompatibility in genetic background may contribute to human 46, XY gonadal dysgenesis in association with SRY mutations as a mechanism of infertility in Swyer’s syndrome (Michala et al. 2008).

  5. 5.

    In genus Akodon , distinct Sry alleles coexist within the same species. In A. azarae, for example, the SRY sequences obtained from two XY females differ at consensus position 13 of the HMG box (i.e., corresponding to position 13 in mouse Sry and position 68 in human SRY): Met or Val (Sánchez et al. 2010). This side chain, designated the cantilever, inserts between DNA base pairs at a site of sharp DNA bending (King and Weiss 1993; Haqq et al. 1994; Murphy et al. 2001) and is conserved as Met, Phe, Ile, or Leu among therian Querymammals (substitution by Ala or Thr blocks specific DNA binding (Weiss et al. 1997). We speculate that the Val cantilever is non-functional and underlies, at least in part, the high percentage of XY sex reversal in this population.

  6. 6.

    The term edge of chaos originally pertained to transition phenomena in cellular automata capable of universal computation (Langton 1990). Stimulated by innovative evolutionary models (Kauffman and Johnsen 1991), this notion provides a general metaphor for critical boundaries between organization and dysgenesis in biological systems, including cellular differentiation (Shmulevich et al. 2005). Dynamic competition between male- and female-specific nonlinear GRNs in the nascent gonad encompasses alternative basins of attraction, respectively, leading to Sertoli- or granulosa cell fates.

Abbreviations

ARD:

Alanine-rich domain

DDA:

Distance distribution analysis

FRET:

Fluorescence resonance energy transfer

GRD:

Glutamine-rich domain

GRN:

Gene regulatory network

GRT:

Gln-rich tract

HMG:

High mobility group

PCR:

Polymerase chain reaction

q-PCR:

Quantitative reverse-transcription PCR

Sox:

Sry-related HMG box

Sry:

Sex-determining region of the Y chromosome

TAD:

Transcriptional activation domain

TDF:

Testis-determining factor

TES:

Testis-specific enhancer

TF:

Transcription factor

tr-FRET:

Time-resolved FRET

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Acknowledgments

We thank JD Racca and NB Phillips (CWRU) for discussion and communication of results prior to publication; E Haas (Bar-Ilan University) for collaborative fluorescence studies; C-Y King, JD Radek, and A Jansco-Radek for participation in early stages of this work; J Graves (University of Melbourne) for her encouragement and scientific example; Robin Lovell-Badge for his astute critique and gracious advice; and PK Donahoe (Massachusetts General Hospital and Harvard Medical School) for cell line CH34 and advice throughout these studies. MAW is grateful to B. Baker (HHMI Janelia Farms) and the late FA Jenkins Jr (Harvard University) for inspiration. The present studies were supported in part by a grant from the US National Institutes of Health (GM080505).

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  1. Thermalin Diabetes, LLC, 10000, Cedar Rd, Cleveland, OH, 44106, USA

    Paul Sequeira

  2. Department of Biochemistry, Case Western Reserve University School of Medicine, 10900, Euclid Avenue, Cleveland, OH, 44106, USA

    Paul Sequeira, Yen-Shan Chen & Michael A. Weiss

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  1. Paul Sequeira
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  2. Yen-Shan Chen
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  3. Michael A. Weiss
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Correspondence to Michael A. Weiss .

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  1. Evolution Biologique et Modélisation I2M UMR 7373, Aix Marseille Université /CNRS, Marseilles, France

    Pierre Pontarotti

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Sequeira, P., Chen, YS., Weiss, M.A. (2015). Mutation-Driven Evolution: Microsatellite Instability Drives Speciation in a Mammalian Taxon. In: Pontarotti, P. (eds) Evolutionary Biology: Biodiversification from Genotype to Phenotype. Springer, Cham. https://doi.org/10.1007/978-3-319-19932-0_8

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