Triad hybridization via a conduit species

Abstract

Introgressive hybridization can affect the evolution of populations in several important ways. It may retard or reverse divergence of species, enable the development of novel traits, enhance the potential for future evolution by elevating levels of standing variation, create new species, and alleviate inbreeding depression in small populations. Most of what is known of contemporary hybridization in nature comes from the study of pairs of species, either coexisting in the same habitat or distributed parapatrically and separated by a hybrid zone. More rarely, three species form an interbreeding complex (triad), reported in vertebrates, insects, and plants. Often, one species acts as a genetic link or conduit for the passage of genes (alleles) between two others that rarely, if ever, hybridize. Demographic and genetic consequences are unknown. Here we report results of a long-term study of interbreeding Darwin's finches on Daphne Major island, Galápagos. Geospiza fortis acted as a conduit for the passage of genes between two others that have never been observed to interbreed on Daphne: Geospiza fuliginosa, a rare immigrant, and Geospiza scandens, a resident. Microsatellite gene flow from G. fortis into G. scandens increased in frequency during 30 y of favorable ecological conditions, resulting in genetic and morphological convergence. G. fortis, G. scandens, and the derived dihybrids and trihybrids experienced approximately equal fitness. Especially relevant to young adaptive radiations, where species differ principally in ecology and behavior, these findings illustrate how new combinations of genes created by hybridization among three species can enhance the potential for evolutionary change.

Keywords: convergence; fitness; introgression; speciation; trihybrids.

Fig. 1.

Gene exchange among three species of Darwin’s finches. The green lines indicate an indirect transfer from G. fuliginosa to G. scandens via G. fortis acting as a conduit. G. fuliginosa is too rare to form an independent breeding population. The principal flow of genes is from G. fortis to G. scandens (blue line).

Fig. 2.

Frequencies of hybrids produced in each year of breeding. Hybrids are expressed as frequencies of the offspring produced in each of the G. fortis groups (G. fortis, Ff [A], FS [B]) and G. scandens groups (G. scandens, SF [C], Sf [D], fS). Regressions are significant for FS and SF frequencies (see Frequencies of Primary Admixtures).

Fig. 3.

Genetic convergence. (A) G. scandens became progressively more similar genetically to G. fortis across five periods (1975 to 1987, 1990 to 1993, 1997 to 1998, 2000 to 2002, 2005 to 2011) separated by years of little or no breeding. The regression relationship of annual mean D_A values on time for the combined data are significant (F_1,4 = 15.30, P = 0.0297, R² adj = 0.78), and has a negative slope of −0.024 ± 0.006 (A). (B–D) Significant regression relationships at three of the individual loci: locus 2.26 (F = 27.92, P = 0.0132, b = −0.048 ± 0.009 SE, R² adj = 0.87), locus 241 (F = 15.06, P = 0.0303, b = −0.057 ± 0.015, R² adj = 0.78), and locus 420 (F = 47.13, P = 0.0063, b = −0.092 ± 0.013, R² adj = 0.92).

Fig. 4.

Beak shape and body size of hybrids (dots) in relation to 99% ellipses around the distributions of G. fuliginosa (green), G. fortis (blue), and G. scandens (pink). (A) G. fuliginosa × G. fortis dihybrids. (B) G. fuliginosa × G. scandens dihybrids. (C) G. fortis × G. scandens dihybrids. (D) Trihybrids: beak pointedness increases from origin to the top, and body size increases from left to right. The smallest trihybrid outlier is fFS, and the other two are FfS.

Fig. 5.

Survival of di- and trihybrids in relation to G. fortis and G. scandens from year 1 in the years 1987 to 2010. (A) Dihybrids Ff (green) and FS (red). (B) Trihybrids FSf + FSf (black) and FfS + fFS (green). (C) Di- and trihybrids SF (blue), Sf (green), and SFf + SfF (black). (D) G. fortis compared with dihybrids and trihybrids with predominant assignment to G. fortis (Ff, FS, FfS, fFS, FSf, fSF).