Evolution of Chilean colonizing populations of Drosophila subobscura: lethal genes and chromosomal arrangements

Abstract

Knowledge of the frequency, distribution, and fate of lethal genes in chromosomal inversions helps to illuminate the evolution of recently founded populations. We analyze the relationship between lethal genes and inversions in two colonizing populations of D. subobscura in Chile. In the ancestral Palearctic populations of this species, lethal genes seem distributed at random on chromosomes. But in colonizing American populations, some lethal genes are associated with specific chromosomal arrangements. Some of these associated lethals were detected only during the first stages of the colonization (O 3?4?2 ), and never thereafter, whereas others have persisted (O 3?4?7 and O 5 ). However, most lethal genes in American populations have been observed only once: they have arisen by novel mutation and soon disappear. Finally, recombination between different inversions has been observed in America. However, the persistence of lethal genes associated with the heterotic inversions O 3?4?7 and O 5 could indicate that recombination inside these inversions is rare.

Recent origin of a chromosomal inversion revealed by its association with nucleotide haplotypes

“…From its point of origin, the inversion had to spread to a huge area as indicated by the presence of haplotype 1 in Montenegro, France and Scandinavia. This expansion of the O 5 inversion is compatible with the levels of gene flow observed in this species in the European and American regions (Latorre et al 1992; Pascual et al 2001; Zivanovic et al 2007; Mestres et al 2009). A sporadic genetic exchange (crossing‐over or gene conversion) could explain the presence of haplotype 2 associated to the O 5 inversion.…”

Molecular evidence to suggest the origin of a colonization: Drosophila subobscura in America

“…association with a lethal gene (Mestres et al 1990(Mestres et al , 1992(Mestres et al , 1995(Mestres et al , 2005(Mestres et al , 2009), though it 116 has proved to be heterotic in these populations (Mestres et al 2001). In an early phase 117 of research we characterized this inversion by sequencing the Odh (Octanol 118 dehydrogenase) gene, which is located inside the O 5 inversion close to its proximal 119 break point (Mestres et al 2004).…”

Inbreeding and thermal adaptation inDrosophila subobscura

“…The second arrangement (O 3+4+22 ) is also common in the Balkans (Krimbas 1993) and can be found in frequencies ranging from 6.5% to 16.7% (Zivanovic et al 2002(Zivanovic et al , 2012Zivanovic 2007;Zivanovic andMestres 2010a, 2011). Maybe despite the inbreeding, they were segregating due to lethal genes trapped inside the O 1 and O 22 inversions, as they are small and recombination inside them is dramatically reduced (Albornoz and Domínguez 1994;Chang and Lin 1995;Chang et al 1996;Yang et al 2002;Mestres et al 2009). However, this possibility is only speculative.…”

“…However, the inbred line with the fixed arrangement O 3+4+7 was really surprising. This arrangement is very uncommon in the Balkan region (Krimbas 1993;Zivanovic et al 1995Zivanovic et al , 2002Zivanovic et al , 2012Zivanovic 2007;Zivanovic andMestres 2010a, 2011), but it is frequent in the Western Mediterranean (Prevosti et al 1984;Krimbas 1993;Orengo and Prevosti 1996;Solé et al 2002;Araúz et al 2009) and American colonizing populations (Prevosti et al 1988(Prevosti et al , 1990Balanyà et al 2003;Mestres et al 2009;Castañeda et al 2013). It was also described in Asia Minor and Israel, but data available from these regions are not recent (Goldschmidt 1956;Götz 1967;Malogolowkin-Cohen and Sperlich 1981).…”