Modeling the two-locus architecture of divergent pollinator adaptation: how variation in SAD paralogs affects fitness and evolutionary divergence in sexually deceptive orchids.

Shuqing Xu,Philipp M Schlüter

doi:10.1002/ece3.1378

Shuqing Xu, Philipp M Schlüter

Open Access

https://doi.org/10.1002/ece3.1378

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Abstract

Divergent selection by pollinators can bring about strong reproductive isolation via changes at few genes of large effect. This has recently been demonstrated in sexually deceptive orchids, where studies (1) quantified the strength of reproductive isolation in the field; (2) identified genes that appear to be causal for reproductive isolation; and (3) demonstrated selection by analysis of natural variation in gene sequence and expression. In a group of closely related Ophrys orchids, specific floral scent components, namely n-alkenes, are the key floral traits that control specific pollinator attraction by chemical mimicry of insect sex pheromones. The genetic basis of species-specific differences in alkene production mainly lies in two biosynthetic genes encoding stearoyl–acyl carrier protein desaturases (SAD) that are associated with floral scent variation and reproductive isolation between closely related species, and evolve under pollinator-mediated selection. However, the implications of this genetic architecture of key floral traits on the evolutionary processes of pollinator adaptation and speciation in this plant group remain unclear. Here, we expand on these recent findings to model scenarios of adaptive evolutionary change at SAD2 and SAD5, their effects on plant fitness (i.e., offspring number), and the dynamics of speciation. Our model suggests that the two-locus architecture of reproductive isolation allows for rapid sympatric speciation by pollinator shift; however, the likelihood of such pollinator-mediated speciation is asymmetric between the two orchid species O. sphegodes and O. exaltata due to different fitness effects of their predominant SAD2 and SAD5 alleles. Our study not only provides insight into pollinator adaptation and speciation mechanisms of sexually deceptive orchids but also demonstrates the power of applying a modeling approach to the study of pollinator-driven ecological speciation.

Highlights

Linking specific genes to fitness differences is one of the main objectives of evolutionary biology, with recent research programs increasingly aiming at uncovering the genes that underlie adaptation and ecological speciation (Lexer and Widmer 2008; Presgraves 2010; Nosil and Schluter 2011; Ostevik et al 2012)
In some orchid populations, SAD1 alleles may contribute to 9-/12-alkene biosynthesis, and SAD6 may sometimes contribute to the production of 7-alkenes (Xu et al 2012a)
Our results show that the potential for pollinator-mediated ecological speciation processes between O. sphegodes and O. exaltata is likely to be asymmetric due to different effect sizes of alleles at SAD2 and SAD5

Summary

Introduction

Linking specific genes to fitness differences is one of the main objectives of evolutionary biology, with recent research programs increasingly aiming at uncovering the genes that underlie adaptation and ecological speciation (Lexer and Widmer 2008; Presgraves 2010; Nosil and Schluter 2011; Ostevik et al 2012). It is important to understand the genetic architecture of phenotypic traits, because it may influence their evolutionary trajectories by facilitating or constraining the way in which traits can be altered by selection. Knowledge of the genetic basis of adaptive traits allows us to infer the accessibility of different evolutionary paths, and the genetic changes and selective pressures that are necessary to effect evolutionary change. Potentially powerful to address questions that are not directly amenable to experimentation, field-derived fitness estimates of specific alleles underlying a 2015 The Authors.

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