Reproductive character displacement allows two sexually deceptive orchids to coexist and attract the same specific pollinator

Salvatore Cozzolino,Donata Cafasso,Giovanni Scopece,Manfred Ayasse,Maria Rosaria Barone Lumaga,Pierluigi Cortis

doi:10.1007/s10682-021-10149-2

Salvatore Cozzolino, Donata Cafasso + Show 4 more

Open Access

https://doi.org/10.1007/s10682-021-10149-2

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Abstract

An increased divergence in characters between species in secondary contact can be shaped by selection against competition for a common resource (ecological character displacement, ECD) or against maladapted hybridization (reproductive character displacement, RCD). These selective pressures can act between incipient species (reinforcement) or well-separated species that already completed the speciation process, but that can still hybridize and produce maladapted hybrids. Here, we investigated two well-separated sexually deceptive orchid species that, unusually, share their specific pollinator. Sympatric individuals of these species are more divergent than allopatric ones in floral characters involved in a mechanical isolating barrier, a pattern suggestive of RCD. To experimentally test this scenario, we built an artificial sympatric population with allopatric individuals. We measured flower characters, genotyped the offspring in natural and artificial sympatry and estimated fertility of hybrids. Different from naturally sympatric individuals, allopatric individuals in artificial sympatry hybridized widely. Hybrids showed lower pollination success and seed viability than parentals. Character displacement did not affect plant pollination success. These findings suggest that RCD evolved between these species to avoid hybridization and that selection on reinforcement may be very strong even in plants with highly specialized pollination.

Highlights

Reproductive isolation can evolve between incipient species as a byproduct of niche divergence and may occur at different degrees of allopatry, parapatry or sympatry (Coyne and Orr 2004)
Molecular analyses showed that none of the fruits collected in 2017 in the natural sympatric population contained hybrid seeds, whilst 9 out of (75%) fruits collected in the artificial sympatric population were of hybrid origin (5 out of 7 on O. chestermanii and 4 out of 5 on O. normanii)
In 2018, molecular analyses showed 8 out of 32 (25%) fruits collected in the artificial sympatric population were of hybrid origin (4 out of 23 fruits collected on O. chestermanii and 4 out of 9 fruits collected on O. normanii)

Summary

Introduction

Reproductive isolation can evolve between incipient species as a byproduct of niche divergence and may occur at different degrees of allopatry, parapatry or sympatry (Coyne and Orr 2004). If hybrids are less fit than parentals, natural selection is expected to favour local phenotypes that minimize gamete waste in interspecific crosses, and secondary contact zones become places where reproductive barriers may continue to evolve and reinforce, completing the speciation process (e.g., Gerhardt 1994; Noor 1995; Rundle and Schluter 1998; Servedio and Noor 2003; Haavie et al 2004; Lemmon 2009; Sobel et al 2010; Roda et al 2017; Spriggs et al 2019) The consequence of this so-called sympatric reinforcement of prezygotic isolation (Dobzhansky 1940), is an increased divergence of sympatric populations of the two incipient species (Noor 1999). While sympatric reinforcement of prezygotic isolation (sensu Dobzhansky 1940) prevents gene flow that would lead to the genetic swamping of the incipient species, RCD relates to species that are already isolated to a degree sufficient to prevent their genetic amalgamation when in contact (Armbruster and Muchhala 2009)

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