Historical Isolation Facilitates Species Radiation by Sexual Selection: Insights from Chorthippus Grasshoppers
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Received: 20 May 2020 | Revised: 29 September 2020 | Accepted: 5 October 2020 DOI: 10.1111/mec.15695 ORIGINAL ARTICLE Historical isolation facilitates species radiation by sexual selection: Insights from Chorthippus grasshoppers Zachary J. Nolen1,2 | Burcin Yildirim1 | Iker Irisarri3,4,5 | Shanlin Liu6,7 | Clara Groot Crego1 | Daniel Buchvaldt Amby6 | Frieder Mayer8 | M. Thomas P. Gilbert9 | Ricardo J. Pereira1,6 1Division of Evolutionary Biology, Faculty of Biology II, Ludwig- Maximilians-Universität Abstract München, München, Germany Theoretical and empirical studies have shown that species radiations are facilitated 2 Department of Biology, Lund University, when a trait under divergent natural selection is also involved in sexual selection. It Lund, Sweden 3Department of Biodiversity and is yet unclear how quick and effective radiations are where assortative mating is un- Evolutionary Biology, Museo Nacional de related to the ecological environment and primarily results from sexual selection. We Ciencias Naturales (MNCN-CSIC), Madrid, Spain address this question using sympatric grasshopper species of the genus Chorthippus, 4Department of Organismal Biology which have evolved strong behavioural isolation while lacking noticeable ecomor- (Systematic Biology), Uppsala University, phological divergence. Mitochondrial genomes suggest that the radiation is relatively Uppsala, Sweden recent, dating to the mid-Pleistocene, which leads to extensive incomplete lineage 5Department of Applied Bioinformatics, Institute for Microbiology and Genetics, sorting throughout the mitochondrial and nuclear genomes. Nuclear data shows University of Goettingen, Campus Institute that hybrids are absent in sympatric localities but that all species have experienced Data Science, Goettingen, Germany 6Natural History Museum of Denmark, gene flow, confirming that reproductive isolation is strong but remains incomplete. University of Copenhagen, Copenhagen, Demographic modelling is most consistent with a long period of geographic isola- Denmark tion, followed by secondary contact and extensive introgression. Such initial periods 7College of Plant Protection, China Agricultural University, Beijing, China of geographic isolation might facilitate the association between male signaling and 8Museum für Naturkunde – Leibniz Institute female preference, permitting the coexistence of sympatric species that are geneti- for Evolution and Biodiversity Science, Berlin, Germany cally, morphologically, and ecologically similar, but otherwise behave mostly as good 9GLOBE Institute, University of biological species. Copenhagen, Copenhagen, Denmark KEYWORDS Correspondence Ricardo J. Pereira, Division of Evolutionary diversification, gene flow, hybridization, sexual selection, speciation Biology, Faculty of Biology II, Ludwig- Maximilians-Universität München, Planegg- Martinsried, Germany. Email: [email protected] Funding information H2020 Marie Skłodowska-Curie Actions, Grant/Award Number: 658706 This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes. © 2020 The Authors. Molecular Ecology published by John Wiley & Sons Ltd Molecular Ecology. 2020;29:4985–5002. wileyonlinelibrary.com/journal/mec | 4985 4986 | NOLEN ET AL. 1 | INTRODUCTION female preference. However, the operational difficulty of classi- fying a radiation as nonecological comes from the impossibility of Speciation begins when populations accumulate genetic differences measuring all ecological attributes of species, which means that eco- that result in reproductive barriers (Mayr, 1963), such as incompati- logical differences can escape detection when they are difficult to ble mating signals that prevent interbreeding, incompatible ecologi- study, when their relative contribution to reproductive isolation is cal interactions that render hybrids unfit in either extrinsic parental small, or when they are restricted to certain life stages (Rundell & habitat, or incompatible gene interactions that cause intrinsic hybrid Price, 2009). Although these systems have received less attention dysfunction (Presgraves, 2010). Although multiple barriers are ex- from evolutionary biologists relative to well-studied ecological ra- pected to become coupled during the speciation process (Butlin & diations, nonecological radiations can lead to similar burst of spe- Smadja, 2018), behavioural barriers usually evolve early during di- cies that maintain behavioural barriers, despite lacking geographic vergence, leading taxonomists to rank their importance “far ahead and ecological isolation. The highest rate of speciation recorded of all others” (Mayr, 1963). Although sexual selection is generally in arthropods occurs in Laupala Hawaiian crickets (Mendelson & accepted as an important driving force of such early behavioural Shaw, 2005), where species remain reproductively isolated due to incompatibilities, it is thought to result in assortative mating only pulse rate of male courtship songs associated to female preference when acting in concert with divergent natural selection (Servedio for specific pulse rates (Otte, 1994), suggesting that sexual selec- & Boughman, 2017). Thus, it is still unclear how efficient species ra- tion on these traits may be the driver of this radiation. Although diations are when assortative mating is unrelated to the ecological these systems are common in nature, the demographic conditions environment, and which demographic scenarios may favour the evo- associated to their radiation remain poorly understood. In particular, lution of assortative mating in the first place. it is still unclear how rapid these radiations can be, if behavioural Emblematic examples of species radiations driven by diver- isolation alone can prevent hybridization in sympatry, and whether gent natural selection, termed “ecological radiations” (Nosil, 2012; behavioural isolation evolved in the face of continuous gene flow or Schluter, 2000), have been a major focus of evolutionary studies be- during historical periods of geographic isolation. cause they shed light onto the selective forces and the demographic Chorthippus grasshoppers are ideally suited to answer such scenarios that result in stable behavioural incompatibilities in the questions and to provide general insights into whether sexual se- face of homogenizing gene flow. For example, in radiations of sym- lection can maintain species boundaries without a primary role of patric species of Darwin finches (Grant & Grant, 2011), cichlid fishes environmental factors (Mayer et al., 2010). This genus comprises (Carleton & Kocher, 2001), and butterflies (Jiggins, 2017), consistent around 230 nominal species (Cigliano et al., 2020), including sev- phenotype-environment correlations suggest the repeated action of eral species groups of morphologically similar species such as the natural selection driven by different ecological niches (seed sizes, biguttulus group (Harz, 1975; Figure 1) that conform to several ex- water clarity, or antipredator strategies) shaping trait values (beak pectations for species mainly separated by sexual selection (Panhuis shape, opsins, and colour pattern). Because such ecologically rele- et al., 2001). First, these species strongly differ in male songs and vant traits also function as mating cues, behavioural isolation may in co-evolving female acoustic preferences (Perdeck, 1958; von emerge as a byproduct of divergent natural selection (Langerhans & Helversen & von Helversen, 1994), as well as in cuticular hydro- Riesch, 2013; Servedio et al., 2011; Smadja & Butlin, 2011). carbons (Finck et al., 2016), all genetically inherited. Second, this Nevertheless, species radiations may also occur without the clear coupling of male song and female preference is sufficient to result evidence of divergent natural selection. In these so-called “noneco- in prezygotic isolation where species are sympatric (von Helversen logical” radiations (Mayer et al., 2010; Rundell & Price, 2009), sym- & von Helversen, 1994), so that hybrids are rarely found in nature patric species do not occupy different ecological niches (Gillespie (Baur, 2006; Jacobs, 1963; Perdeck, 1958). Third, there is little ge- et al., 2001), and did not diverge in ecologically relevant traits netic differentiation between species (Hawlitschek et al., 2017; (Gillespie et al., 2020; Schluter, 2000). Instead, sexual selection is Mason et al., 1995), suggesting rapid divergence. Finally, there is no assumed to be the primary driving force in the divergence between reduction in F1 hybrid viability or fertility caused by Dobzhansky- populations (Panhuis et al., 2001; Ritchie, 2007). Although the sexual Muller incompatibilities (Perdeck, 1958; Saldamando, Tatsuta, & selective pressures (e.g., female preference) are similar in sister taxa Butlin, 2005; but see Finck & Ronacher, 2017). Yet, hybrid fitness at early stages of divergence, the order that sexual traits (e.g., male is reduced in F1 males due to an intermediate song that is not ap- signalling) arise and become fixed is stochastic, resulting in indepen- pealing to either parental female nor to their F1 sisters, leaving them dent coevolution of signal and preference within each lineage, and “behaviourally sterile” (Gottsberger & Mayer, 2007, 2019). It is still causing behavioural isolation upon secondary contact (i.e., “muta- unclear whether