Postzygotic isolation drives genomic speciation between highly crypticHypocnemisantbirds from Amazonia

Abstract

How species evolve reproductive isolation in the species-rich Amazon basin is poorly understood in vertebrates. Here, we sequenced a reference genome and used a genome-wide sample of SNPs to analyze a hybrid zone between two highly cryptic species of Hypocnemis warbling-antbirds-the Rondonia warbling-antbird (H. ochrogyna) and Spix's warbling-antbird (H. striata)-in a headwater region of southern Amazonia. We found that both species commonly hybridize, producing F 1 s and a variety of backcrosses with each species but we detected only one F 2-like hybrid. Patterns of heterozygosity, hybrid index, and interchromosomal linkage disequilibrium in hybrid populations closely match expectations under strong postzygotic isolation. Hybrid zone width (15.4 km) was much narrower than expected (211 km) indicating strong selection against hybrids. A remarkably high degree of concordance in cline centers and widths across loci, and a lack of reduced interspecific F st between populations close to versus far from the contact zone, suggest that genetic incompatibilities have rendered most of the genome immune to introgression. These results support intrinsic postzygotic isolation as a driver of speciation in a moderately young cryptic species pair from the Amazon and suggest that species richness of the Amazon may be grossly underestimated.

Hybridization and the Coexistence of Species

“…These other possibilities start to become likely when assortative mating is reduced from complete to merely extremely strong, for example a 300 times greater preference (when W hyb = 1) of a female for a male of her own species compared to a male of the other species. Collapse of two species into a hybrid population despite strong assortative mating has also been observed using other modelling approaches [19,27–29], although the approach used here differs from earlier approaches by incorporating ecological differentiation and the possibility of population decline.…”

Evaluating evidence of mitonuclear incompatibilities with the sex chromosomes in an avian hybrid zone

“…(2018) and Cronemberger et al. (2020), but with modifications for the behavior of sex‐linked genotypes and including mito‐type information (see Fig. 1 and Table S5).…”

Non-parallel morphological divergence following colonization of a new host plant

“…insect host races inhabiting different discrete plant niches. Close congeners inhabiting different niches may be poorly adapted to the alternative environment (Rundle & Nosil, 2005, Nilsson et al, 2017, Cronemberger et al, 2020, Martin et al, 2020, which may lead to reinforcement (Servedio & Noor, 2003) and character displacement with stronger differences in traits involved in mate choice (Hinojosa et al, 2020). While parallel divergence is expected (which was not certified by peer review) is the author/funder.…”

“…insect host races inhabiting different discrete plant niches. Close congeners inhabiting different niches may be poorly adapted to the alternative environment (Rundle & Nosil, 2005, Nilsson et al, 2017, Cronemberger et al, 2020, Martin et al, 2020), which may lead to reinforcement (Servedio & Noor, 2003) and character displacement with stronger differences in traits involved in mate choice (Hinojosa et al, 2020). While parallel divergence is expected for ecologically selected traits (Figure 1A), either parallel- or nonparallel character displacement (Figure 1B-C) or reduced divergence due to introgression (Figure 1D) could be expected for sexually selected traits that are not strongly coupled with host plant use.…”

“…This could be particularly evident when different populations of the diverging species are inhabiting discrete niches, like in the case of insect host races. Close congeners inhabiting different niches may be poorly adapted to the alternative environment (Rundle and Nosil 2005;Nilsson et al 2017;Cronemberger et al 2020;Martin et al 2020), which may lead to reinforcement (Servedio and Noor 2003) and character displacement with stronger differences in traits involved in mate choice (Hinojosa et al 2020). While parallel divergence is expected for ecologically selected traits (Fig.…”