Morning glory species co-occurrence is associated with asymmetrically decreased and cascading reproductive isolation

Abstract

Hybridization between species can affect the strength of the reproductive barriers that separate those species. Two extensions of this effect are (1) the expectation that asymmetric hybridization or gene flow will have asymmetric effects on reproductive barrier strength and (2) the expectation that local hybridization will affect only local reproductive barrier strength and could therefore alter within-species compatibility. We tested these hypotheses in a pair of morning glory species that exhibit asymmetric gene flow from highly selfing Ipomoea lacunosa into mixed-mating Ipomoea cordatotriloba in regions where they co-occur. Because of the direction of this gene flow, we predicted that reproductive barrier strength would be more strongly affected in I. cordatotriloba than I. lacunosa. We also predicted that changes to reproductive barriers in sympatric I. cordatotriloba populations would affect compatibility with allopatric populations of that species. We tested these predictions by measuring the strength of a reproductive barrier to seed set across the species' ranges. Consistent with our first prediction, we found that sympatric and allopatric I. lacunosa produce the same number of seeds in crosses with I. cordatotriloba, whereas crosses between sympatric I. cordatotriloba and I. lacunosa are more successful than crosses between allopatric I. cordatotriloba and I. lacunosa. This difference in compatibility appears to reflect an asymmetric decrease in the strength of the barrier to seed set in sympatric I. cordatotriloba, which could be caused by I. lacunosa alleles that have introgressed into I. cordatotriloba. We further demonstrated that changes to sympatric I. cordatotriloba have decreased its ability to produce seeds with allopatric populations of the same species, in line with our second prediction. Thus, in a manner analogous to cascade reinforcement, we suggest that introgression associated with hybridization not only influences between-species isolation but can also contribute to isolation within a species.

Keywords: Gene flow; Ipomoea; hybridization; mating system; reproductive barriers; speciation.

Figure 1

Information about our study species. (A) Map showing the approximate distributions ofI. lacunosa(LAC, green) andI. cordatotriloba(COR, purple) in North America. This map was redrawn based on Khoury et al. (2015) and generally matches collection records from the United States (USDA, NRCS2019). (B) A typical allopatricI. cordatotrilobaflower. (C) A typicalI. lacunosaflower. (D) Map showing the locations of populations used in this study (see Table S1 for details).

Figure 2

The effect of species combination on seed set. The number of seeds produced by different types of crosses (ovule parent × pollen parent; C =I. cordatotrilobaand L =I. lacunosa). Each box is proportional to the number of fruits that contained indicated number of seeds after pollination. Dashed lines represent cases in which there were no fruits with a particular seed number.

Figure 3

Species co‐occurrence affects interspecific cross success. (A) The proportion of interspecific crosses that set at least one mature seed. (B) The mean and 95% confidence intervals (based on bootstrap percentiles) for the mean number of seeds produced by different types of interspecific crosses (from left to right): both species are allopatric (A), both species are sympatric (S), allopatricI. cordatotriloba(COR) and anyI. lacunosa(LAC), sympatricI. cordatotrilobaand anyI. lacunosa, allopatricI. lacunosaand anyI. cordatotriloba, sympatricI. lacunosaand anyI. cordatotriloba.^* P< 0.05;^*** P< 0.001.

Figure 4

The success of crosses withinI. cordatotriloba, but not withinI. lacunosa, depends on species co‐occurrence. The proportion of fruits with at least one mature seed set after crosses withinI. cordatotriloba(A) and withinI. lacunosa(B) and the mean number of seeds produced by crosses withinI. cordatotriloba(C) and withinI. lacunosa(D). In panels C and D, each point represents the mean number of seeds produced by five to six crosses made with same individuals and means and 95% confidence intervals for those means are also plotted. Means not sharing any letter within a panel are significantly different atP< 0.05.