Domestication is associated with increased interspecific hybrid compatibility in landfowl (order: Galliformes)

Abstract

Some species are able to hybridize despite being exceptionally diverged. The causes of this variation in accumulation of reproductive isolation remain poorly understood, and domestication as an impetus or hindrance to reproductive isolation remains to be characterized. In this study, we investigated the role of divergence time, domestication, and mismatches in morphology, habitat, and clutch size among hybridizing species on reproductive isolation in the bird order Galliformes. We compiled and analyzed hybridization occurrences from literature and recorded measures of postzygotic reproductive isolation. We used a text-mining approach leveraging a historical aviculture magazine to quantify the degree of domestication across species. We obtained divergence time, morphology, habitat, and clutch size data from open sources. We found 123 species pairs (involving 77 species) with known offspring fertility (sterile, only males fertile, or both sexes fertile). We found that divergence time and clutch size were significant predictors of reproductive isolation (McFadden's Pseudo-R2 = 0.59), but not habitat or morphological mismatch. Perhaps most interesting, we found a significant relationship between domestication and reproductive compatibility after correcting for phylogeny, removing extreme values, and addressing potential biases (F1,74 = 5.43, R2 = 0.06, P-value = 0.02). We speculate that the genetic architecture and disruption in selective reproductive regimes associated with domestication may impact reproductive isolation, causing domesticated species to be more reproductively labile.

Keywords: Haldane’s Rule; artificial selection; bird; reproductive barriers; speciation.

Fig. 1.

Hybridizations with documented offspring fertility in the bird order Galliformes. The orange links represent crosses where offspring (some or all) are fertile. The blue links represent crosses in which all offspring are sterile. The phylogeny is from the TimeTree database (Kumar et al. 2022)..

Fig. 2.

Added variable plots of the partial correlation between divergence and reproductive isolation and clutch size difference and reproductive isolation. Each circle represents one of the crosses, and the blue line is the line of best fit.

Fig. 3.

Logistic regressions of Haldane’s Rule (A) and the time to speciate (B). A) 1 represents hybrids where only the males are fertile, and 0 represents hybrids where both sexes are fertile. The blue line represents the divergence time where there is an equal probability of a cross resulting in a hybrid where both sexes are fertile or only the males are fertile. B) 1 represents crosses resulting in a hybrid with any fertility (both and only males), and 0 represents sterility of both sexes. The orange line represents the divergence time with an equal probability of a cross resulting in a sterile or fertile hybrid offspring.

Fig. 4.

The phylogenetic generalized linear model between reproductive isolation and domestication index. The orange line represents the best fit of all data, while the blue line represents the best fit, excluding the 10 most and 12 least domesticated species.

Fig. 5.

Mean residuals of the five species with the most hybridization records with documented offspring fertility plotted against a null distribution of 10,000 samplings of 13 species (Gallus gallus).