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Avian sex, sex chromosomes, and dosage compensation in the age of genomics

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Abstract

Comparisons of the sex chromosome systems in birds and mammals are widening our view and deepening our understanding of vertebrate sex chromosome organization, function, and evolution. Birds have a very conserved ZW system of sex determination in which males have two copies of a large, gene-rich Z chromosome, and females have a single Z and a female-specific W chromosome. The avian ZW system is quite the reverse of the well-studied mammalian XY chromosome system, and evolved independently from different autosomal blocs. Despite the different gene content of mammal and bird sex chromosomes, there are many parallels. Genes on the bird Z and the mammal X have both undergone selection for male-advantage functions, and there has been amplification of male-advantage genes and accumulation of LINEs. The bird W and mammal Y have both undergone extensive degradation, but some birds retain early stages and some mammals terminal stages of the process, suggesting that the process is more advanced in mammals. Different sex-determining genes, DMRT1 and SRY, define the ZW and XY systems, but DMRT1 is involved in downstream events in mammals. Birds show strong cell autonomous specification of somatic sex differences in ZZ and ZW tissue, but there is growing evidence for direct X chromosome effects on sexual phenotype in mammals. Dosage compensation in birds appears to be phenotypically and molecularly quite different from X inactivation, being partial and gene-specific, but both systems use tools from the same molecular toolbox and there are some signs that galliform birds represent an early stage in the evolution of a coordinated system.

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Abbreviations

ATP5A1:

ATP synthase, H+ transporting, mitochondrial F1 complex

CHD:

Chromodomain helicase DNA binding protein

DMRT1 (Dmrt1 in mice):

Doublesex and Mab3 related transcription factor

DMY:

DM domain containing gene on the Y chromosome in medaka fish

DMW:

DM domain containing gene on the W chromosome in Xenpous laevis

FET-1:

Female-expressed transcript

FEM1c:

Chicken homologue of C. elegans fem-1

FISH:

Fluorescence in situ hybridization

FOXL2:

Forkhead box L2

GGA1:

Gallus gallus chromosome 1

H4:

Histone H4

HINTW:

Histidine triad nucleotide-binding protein 1

LINEs:

Long interspersed nuclear elements

MLH1:

Homologue of C. elegans protein MLH-1

MHM:

Male hypermethylated region

MY, MYA:

Million years (ago)

RNAi:

Interfering RNA

RSPO1:

Respondin 1

SOX3, SOX9:

SRY-like HMG box-containing genes 3 and 9

SRY:

Sex-determining region on the Y

WNT4:

Wingless-type MMTV integration site, family member 4

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  1. LaTrobe Institute of Molecular Science, La Trobe University, Kingsbury Drive, Bundoora, Melbourne, VIC, 3186, Australia

    Jennifer A. Marshall Graves

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  1. Jennifer A. Marshall Graves
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Correspondence to Jennifer A. Marshall Graves.

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Graves, J.A.M. Avian sex, sex chromosomes, and dosage compensation in the age of genomics. Chromosome Res 22, 45–57 (2014). https://doi.org/10.1007/s10577-014-9409-9

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