Nucleotide diversity in 50kb sliding windows along chromosome 7 for six species of Estrildid finches

Nucleotide diversity in 50kb sliding windows along chromosome 7 for six species of Estrildid finches

Population divergence involves not just molecular changes to DNA composition but also physical rearrangements to genome architecture. Chromosome inversion, one class of chromosomal rearrangement, are powerful recombination modifiers often observed as fixed differences between species and polymorphisms segregating within species. Empirical studies have alternately attributed to chromosome inversions a role in sex chromosome evolution, supergene formation, local adaptation, and reproductive isolation. While birds have long been used to study the roles played by behavior and ecology in speciation, little attention has been given to the contribution of chromosome inversions - which are numerous - to avian diversification. My research is therefore focused upon better understanding the process of speciation with gene flow and the evolutionary forces driving chromosome inversion evolution in birds.


Chromosome inversion evolution in Passeriformes

Why do some taxa have more inversion differences than others? The answer to this question remains largely enigmatic despite nearly a century of study. Using karyotype records for over 400 species from 59 families in the most species-rich group of birds (order Passeriformes), I examine support for alternative theoretical models of inversion evolution that rest on contradictory predictions regarding the likelihood of inversion fixation and variance in the speciation history, demography, and ecology of species. I find that inversions are common and likely evolving because they are adaptive. The extent of inversion differentiation between passerine species is best predicted by a model in which inversions are selected for during speciation when gene flow occurs before reproductive isolation is complete. 


Top: Bill color variation across the range of the long-tailed finch ( Poephila acuticauda acuticauda , left; hybrid individual, center;  P. a. hecki , right.). Population sampling in northern Australia for admixture analysis. Sites are color coded by mean bill color. See Griffith and Hooper (2017).

Top: Bill color variation across the range of the long-tailed finch (Poephila acuticauda acuticauda, left; hybrid individual, center; P. a. hecki, right.). Population sampling in northern Australia for admixture analysis. Sites are color coded by mean bill color. See Griffith and Hooper (2017).

Effective migration surfaces for the sex chromosomes across the range of the long-tailed finch (circles) and black-throated finch ( Poephila cincta;  stars). Color gradient depicts geographic areas that are barriers to effective genetic migration (orange) compared to areas of average (white) or elevated migration (blue). This approach highlights the strength of the Z chromosome as a barrier to migration between long-tailed finch subspecies. See Hooper et al. (2018).

Effective migration surfaces for the sex chromosomes across the range of the long-tailed finch (circles) and black-throated finch (Poephila cincta; stars). Color gradient depicts geographic areas that are barriers to effective genetic migration (orange) compared to areas of average (white) or elevated migration (blue). This approach highlights the strength of the Z chromosome as a barrier to migration between long-tailed finch subspecies. See Hooper et al. (2018).



Speciation genomics in the Australian grassfinches

The Australian grassfinches (family Estrildidae) exhibit one of the highest rates of pericentric inversion fixation observed in passerines (Hooper and Price, 2015; 2017). I am using genomic sequence data from a clade of 14 grassfinch species, including subspecies for 8 of which, in order to 1) recover the phylogenetic relationships of this recalcitrant group, 2) examine the frequency of speciation with gene flow, and 3) characterize the history of chromosomal inversion evolution between taxa and the evolutionary context in which these rearrangements have occurred.

Variation in the rate of chromosome inversion fixation across  Passeriformes  using 411 species with karyotype data. Warmer colors correspond to faster rates of inversion fixation. Adapted from Hooper and Price (2017 ).

Variation in the rate of chromosome inversion fixation across Passeriformes using 411 species with karyotype data. Warmer colors correspond to faster rates of inversion fixation. Adapted from Hooper and Price (2017).


Chromosome inversions and reproductive isolation in an avian hybrid zone

The long-tailed finch (Poephila acuticauda) is a species of songbird endemic to the northern tropics of Australia and comprises two hybridizing subspecies that differ primarily in bill color: yellow in the western ssp. acuticauda and red in the eastern ssp. hecki. The subspecies meet, mate, and produce orange-billed hybrids restricted to a narrow zone of admixture (<150km; Griffith and Hooper 2017). Intriguingly, we find that the center of primary genetic admixture between subspecies is displaced, however, some 350km to the west of this zone of bill color mixing and is mediated by inversion differences on the Z chromosome where 99.5% of genetic differences between subspecies reside (Hooper et al. 2018). We are using this hybrid zone to investigate the strength and basis of reproductive isolation between subspecies, the genes underlying both bill color and sperm variation, and the contribution of Z chromosome inversions to these processes.

We are currently using a combination of analytical approaches in tandem (comparative and functional genomics, proteomics, as well as behavioral and developmental studies of parental taxa and hybrids in both the wild and in captivity) to shed light on the process of speciation with gene flow using the long-tailed finch as an emerging model system.

 

Thirteen members of the Australian grassfinches under study. . Top row, left to right: Long-tailed finch ( Poephila acuticauda ), Black-throated finch ( P. cincta ), Masked finch ( P. personata ), Zebra finch ( Taeniopygia guttata ), Double-barred finch ( Stizoptera bichenovii ). Middle row, left to right: Star finch ( Bathilda ruficauda ), Plum-headed finch ( Aidemosyne modesta ), Painted finch ( Emblema pictum ), Red-browed finch ( Neochmia temporalis ), Crimson finch ( N. phaeton ). Bottom row, left to right: Diamond firetail ( Stagonopleura guttata ), Beautiful firetail ( S. bella ), Red-eared firetail ( S. oculata ).  Original artwork courtesy of the incredibly talented A. E. Johnson.

Thirteen members of the Australian grassfinches under study..
Top row, left to right: Long-tailed finch (Poephila acuticauda), Black-throated finch (P. cincta), Masked finch (P. personata), Zebra finch (Taeniopygia guttata), Double-barred finch (Stizoptera bichenovii). Middle row, left to right: Star finch (Bathilda ruficauda), Plum-headed finch (Aidemosyne modesta), Painted finch (Emblema pictum), Red-browed finch (Neochmia temporalis), Crimson finch (N. phaeton). Bottom row, left to right: Diamond firetail (Stagonopleura guttata), Beautiful firetail (S. bella), Red-eared firetail (S. oculata).
Original artwork courtesy of the incredibly talented A. E. Johnson.