Insights into avian molecular cytogenetics-with reptilian comparisons

Abstract

In last 100 years or so, much information has been accumulated on avian karyology, genetics, physiology, biochemistry and evolution. The chicken genome project generated genomic resources used in comparative studies, elucidating fundamental evolutionary processes, much of it funded by the economic importance of domestic fowl (which are also excellent model species in many areas). Studying karyotypes and whole genome sequences revealed population processes, evolutionary biology, and genome function, uncovering the role of repetitive sequences, transposable elements and gene family expansion. Knowledge of the function of many genes and non-expressed or identified regulatory components is however still lacking. Birds (Aves) are diverse, have striking adaptations for flight, migration and survival and inhabit all continents most islands. They also have a unique karyotype with ~ 10 macrochromosomes and ~ 30 microchromosomes that are smaller than other reptiles. Classified into Palaeognathae and Neognathae they are evolutionarily close, and a subset of reptiles. Here we overview avian molecular cytogenetics with reptilian comparisons, shedding light on their karyotypes and genome structure features. We consider avian evolution, then avian (followed by reptilian) karyotypes and genomic features. We consider synteny disruptions, centromere repositioning, and repetitive elements before turning to comparative avian and reptilian genomics. In this context, we review comparative cytogenetics and genome mapping in birds as well as Z- and W-chromosomes and sex determination. Finally, we give examples of pivotal research areas in avian and reptilian cytogenomics, particularly physical mapping and map integration of sex chromosomal genes, comparative genomics of chicken, turkey and zebra finch, California condor cytogenomics as well as some peculiar cytogenetic and evolutionary examples. We conclude that comparative molecular studies and improving resources continually contribute to new approaches in population biology, developmental biology, physiology, disease ecology, systematics, evolution and phylogenetic systematics orientation. This also produces genetic mapping information for chromosomes active in rearrangements during the course of evolution. Further insights into mutation, selection and adaptation of vertebrate genomes will benefit from these studies including physical and online resources for the further elaboration of comparative genomics approaches for many fundamental biological questions.

Keywords: Avian; Bird; Comparative genomics; Cytogenetics; Cytogenomics; Evolution; Genome; Reptile; Sex chromosomes.

Fig. 1

Vertebrate phylogeny and sex determination modes in different taxa. The phylogenetic tree was sourced from TimeTree databases [22] using the following species representing the major clades, Danio rerio (fish), Gallus gallus (birds), Homo sapiens (mammalians), Xenopus tropicalis (amphibians), Caretta caretta (turtles), Pantherophis guttatus (snakes), Anolis carolinensis (lizards), and Crocodylus palustris (Crocodilians). * = Female heterogamety, # Male heterogamety and ✦ = Temperature-dependent sex determination (TSD). Right hand side: Evolutionary relationships and divergence periods of extinct and extant birds. According to molecular clocks, the shaded region in Neoaves denotes the time when the majority of ordinal and superordinal lineages split. Paleontological evidence suggests that the lineages of Mesozoic birds and Archaeopteryx ended arbitrarily at the Cretaceous/Tertiary boundary; however, some lineages may have vanished earlier. (The shown timescale and branches are adapted from [23]; bird silhouettes are sourced from Wikimedia Commons and conform to public domain or CC licenses)

Fig. 2

Chicken sex chromosome G-banded ideogram displaying the shared genes between the Z and PAR on the W chromosome as well as the cytological position of sex determining candidate genes (bold). (adapted from [19]; *Sazanov et al. [169]; **Sazanov et al. [170])