Slow evolutionary loss of the potential for interspecific hybridization in birds: a manifestation of slow regulatory evolution.

Abstract

Birds have lost the potential for interspecific hybridization slowly. This inference emerges from protein comparisons made on 36 pairs of bird species capable of hybridization. Micro-complement fixation tests show that hybridizable pairs of bird species differ by an average of 12 units of albumin immunological distance and 25 units of transferrin immunological distance. As these proteins evolve at a known and rather steady rate, it is inferred that the average hybridizable species pair diverged from a common ancestor about 22 million years ago. The corresponding period for frog species pairs capable of hybridization is about 21 million years, while for hybridizable placental mammals it is only 2 to 3 million years. Thus birds resemble frogs in having lost the potential for interspecific hybridization about 10 times as slowly as have mammals.Birds have also been evolving very slowly at the anatomical level, particularly within the last 25 million years, according to Simpson, Romer, and many other vertebrate zoologists. In this respect they resemble frogs and differ from placental mammals, which have been undergoing unusually rapid anatomical evolution. Chromosomal evolution is also thought to have proceeded very slowly in both birds and frogs, relative to mammals.The above observations are consistent with the hypothesis that evolutionary changes in regulatory systems, that is, changes in the patterns of gene expression, provide the basis for both anatomical evolution and the evolutionary loss of hybridization potential.

Patterns of Reproductive Isolation in Three Angiosperm Genera

“…Second, in a number of animal taxa, prezygotic isolation evolves faster than postzygotic reproductive isolation (Blair 1964;Prager and Wilson 1975;Coyne and Orr 1989;Gleason and Ritchie 1998;Mendelson 2003), indicating that prezygotic mechanisms may be more critical in the initial development of isolation between incipient animal species. The faster evolution of prezygotic mechanisms in animals has also been interpreted as evidence for strong sexual selection acting on prezygotic traits (Gleason and Ritchie 1998).…”

Bird song, ecology and speciation

“…In many instances song differences probably prevent hybridization among species that are fully capable of producing viable and fertile offspring (Prager & Wilson 1975;Grant & Grant 1997a;Baker & Boylan 1999). In addition to the role of song in mate selection at the species level, female mate preferences may also be influenced by intraspecific variation in song (figure 1).…”

Gene Regulatory Evolution During Speciation in a Songbird

“…On the other hand, even crosses between relatively young mouse subspecies (, 0.5 million years) exhibit hybrid sterility and misexpression (Mack et al 2016). Given that there is no evidence of reproductive incompatibility between the zebra finch subspecies and that postzygotic isolation takes a relatively long time to evolve in birds (Prager and Wilson 1975), our results suggest that misexpression may accumulate after the origin of reproductive incompatibilities or may directly contribute to the origin of incompatibilities.…”

“…Therefore, in terms of gene expression, we may expect to see faster expression evolution in Z-linked genes and a tendency for Z-linked genes to be misexpressed in hybrids. Second, the evolution of reproductive isolation is protracted in birds relative to other taxa (Prager and Wilson 1975;Fitzpatrick 2004;Price 2008). Astoundingly, fully fertile hybrids have been documented from bird species that have diverged for up to 10 million years (Tubaro and Lijtmaer 2002;Lijtmaer et al 2003;Price 2008;Arrieta et al 2013).…”