Conservation implications of asymmetric introgression and reproductive barriers in a rare primrose species

Abstract

Background: Primula is a large genus of flowering herbs well known for their heterostyly. Currently few natural hybrids are known and reproductive barriers in this genus in the wild have received little attention. However, there is instance of hybridization between rare and widely-spread species, and conservation implications of such situation is poorly understood. In the present study, we investigated hybridization patterns and reproductive barriers between a wide spread species, Primula poissonii and a rare species P. anisodora, of which only three populations are currently known.

Results: Pollinator-mediated reproductive isolation was strong between parental species but not significant between hybrids and parental species. Hand pollination experiments showed significant reduction of both fruit- and seed-set for heterospecific pollination as compared with conspecific pollination for both parental species. Furthermore, hybrids had higher fruit- and seed-set when pollinated with P. anisodora pollen as opposed to P. poissonii pollen. Microsatellites identified backcrosses to P. anisodora in two of the three populations of P. anisodora, and additionally more individuals of P. anisodora showed introgression from P. poissonii than vice versa.

Conclusions: These results provide evidence for potential genetic swamping of the P. anisodora populations, which could pose a serious threat for this locally endemic species.

Keywords: Asymmetric introgression; Conservation implication; Genetic swamping; Heterostyly; Reproductive isolation.

Fig. 1

Number of transitions between P. poissonii, hybrids and P. anisodora within bouts of three pollinator groups. On the top the currently visited species is indicated, and on the x-axis which species the pollinator had visited immediately before. Pollinators were: Bees (Anthophora sp.), Bumblebees and Butterflies (Aporia bieti). Most visits of butterflies were restricted to P. poissonii with some occasionally visiting hybrids, while bees and bumblebees mostly visited P. anisodora, but were less selective, with several visiting hybrid and P. poissonii flowers

Fig. 2

Transition percentages for three groups of pollinators: Bees (Anthophora sp.), Bumblebees and Butterflies (Aporia bieti) observed in bouts involving P. anisodora, P. poissonii and hybrids. Transition types were categorised as: conspecific (anisodora-anisodora, poissonii-poissonii, hybrid-hybrid), heterospecific (anisodora-poissonii, poissonii-anisodora), or hybrid (anisodora-hybrid, poissonii-hybrid, hybrid-anisodora, hybrid-poissonii). Most transitions were conspecific for all pollinator groups, and heterospecific transitions were relatively rare. Hybrids were much more often included in non-conspecific bouts than the respective other species, suggesting weakening of pollinator-mediated isolation when hybrids are present

Fig. 3

Fruit set (a) and seed numbers per fruits (b) after artificial cross-pollination in 2015 (P. anisodora x P. poissonii) and 2016 (P. anisodora x hybrids &P. poissonii x hybrids). Experiments are separated by cross type involving the different combinations of flower morphs (pin, thrum). For intra-morph crosses, incompatibility effects of the hetorostyly-supergene can be expected. Con-specific crosses produced more fruits/seeds in inter-morph crosses, with thrum/pin having a more pronounced pattern than pin/thrum, while hybrid pollen produced similar amounts of fruit/seeds for both species. For hybrid mothers fruits were only produced from pollination by P. anisodora

Fig. 4

Genotype class assignment of all 168 samples based on the program Structure (a) and 108 samples in the hybrid zone by the program Newhybrids (b)

Fig. 5

Flower morphology and pollinator observation arrays. a, b, c Flower characteristics of P. poissonii, hybrids and P. anisodora with their main shared pollinators in upper-left. d, e, f Pollinator transition observations of arranged species in P. poissonii, hybrids and P. anisodora dominant plots. Bars, 10 mm