vol. 194, no. 2 the american naturalist august 2019 Note A General Explanation for the Persistence of Reproductive Interference Jonathan P. Drury,1,* Christopher N. Anderson,2 Maria B. Cabezas Castillo,3 Jewel Fisher,3 Shawn McEachin,3 and Gregory F. Grether3 1. Department of Biosciences, Durham University, DurhamDH13LE,UnitedKingdom; 2.Departmentof Biological Sciences, Dominican University, River Forest, Illinois 60305; 3. Department of Ecology and Evolutionary Biology, University of California, Los Angeles, California 90095 Submitted September 17, 2018; Accepted February 22, 2019; Electronically published June 13, 2019 Online enhancements: appendix. Dryad data: https://dx.doi.org/10.5061/dryad.63mk0ks. abstract: Reproductive interference is widespread, despite the the- kirch 2008). In the face of such costs, current theory predicts oretical expectation that it should be eliminated by reproductive char- local extinction of one or more species (i.e., reproductive ex- acter displacement (RCD). A possible explanation is that females of clusion; Kuno 1992; Liou and Price 1994; Hochkirch et al. sympatric species are too similar phenotypically for males to distin- 2007; Gröning and Hochkirch 2008; Pfennig and Pfennig guish between them, resulting in a type of evolutionary dilemma or 2012; Kishi and Nakazawa 2013; Grether et al. 2017; but catch-22, in which reproductive interference persists because male see Ruokolainen and Hanski 2016) or evolutionary diver- mate recognition (MR) cannot evolve until female phenotypes diverge gence in traits involved in mate recognition (i.e., reproduc- further, and vice versa. Here we illustrate and test this hypothesis with fl tive character displacement; Brown and Wilson 1956; Hoch- data on rubyspot damsel ies (Hetaerina spp.). First, reproductive iso- fi lation owing to male MR breaks down with increasing interspecific kirch et al. 2007; Burd eld-Steel and Shuker 2011; Pfennig similarity in female phenotypes. Second, comparing allopatric and and Pfennig 2012; Grether et al. 2017). Yet reproductive in- sympatric populations yielded no evidence for RCD, suggesting that terference is widespread in animals (Gröning and Hoch- parallel divergence in female coloration and male MR in allopatry kirch 2008; Shuker and Burdfield-Steel 2017), even among determines the level of reproductive isolation on secondary contact. species that appear to coexist stably (e.g., insects: Hochkirch Whenever reproductive isolation depends on male MR and females et al. 2007; Drury et al. 2015a, 2015b; Shuker et al. 2015; of sympatric species are phenotypically similar, the evolutionary catch- 22 hypothesis offers an explanation for the persistence of reproduc- spiders: Taylor et al. 2017; nematodes: Ting and Cutter 2018; tive interference. amphibians: Pfennig 2003; birds: Veen et al. 2010). Why does reproductive interference persist in spite of its fitness Keywords: reproductive interference, character displacement, local costs (Takakura et al. 2015; Grether et al. 2017)? mate competition, Odonata, mate recognition, evolutionary catch-22. We propose that reproductive interference often persists because of an evolutionary catch-22 arising from interspe- fi fl 1 Introduction ci c sexual con ict. Reproductive interference is likely to carry a net cost for females, but for males, the cost of missed When phenotypically similar species come into contact, in- conspecific mating opportunities is often greater than the terspecific sexual interactions—known as reproductive in- cost of mating with heterospecific females (Shuker et al. terference—can occur (Gröning and Hochkirch 2008). To 2015). The catch-22 is that if females of sympatric species varying degrees, different forms of reproductive interfer- are too similar phenotypically for males to profitably at- ence—such as misdirected courtship, heterospecificmating tempt to distinguish between them, reproductive interfer- attempts, and hybridization—carry fitness costs for indi- ence will persist indefinitely because there is no selection viduals of one or all species involved (Gröning and Hoch- for divergence in male mate recognition (MR) and, conse- quently, no selection on females to diverge phenotypically. Even if males have an incipient ability to distinguish con- specific and heterospecific females, the resulting divergent * Corresponding author; email: [email protected]. ORCIDs: Drury, https://orcid.org/0000-0002-0262-8761; Fisher, https://orcid selection on female phenotypes might be too weak to over- .org/0000-0003-4996-2772; Grether, https://orcid.org/0000-0003-3441-0537. ride stabilizing or convergent selection, because female phe- Am. Nat. 2019. Vol. 194, pp. 000–000. q 2019 by The University of Chicago. 0003-0147/2019/19402-58736$15.00. All rights reserved. 1. An evolutionary catch-22 is a kind of dilemma in which A cannot DOI: 10.1086/704102 evolve until B evolves, and vice versa (Maynard Smith 1983). This content downloaded from 128.097.245.207 on June 27, 2019 12:10:21 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). 000 The American Naturalist notypes that are potentially useful for male MR (e.g., color- tive of the level of reproductive isolation caused by male MR ation) are likely targets of selection in other contexts (e.g., in a clade-wide analysis, confirming that reproductive inter- predation), and closely related sympatric species can be ex- ference arises, at least in part, from similarity in female phe- pected to adapt in similar ways to their common environ- notypes. One species, Hetaerina titia, stands out, both for ment (e.g., Gomez and Théry 2004). being highly variable in wing coloration and for usually ex- The evolutionary catch-22 hypothesis could be rejected periencing low levels of reproductive interference (Drury for a particular taxon by showing that reproductive isola- et al. 2015a, 2015b). To determine how the low levels of re- tion resulting from enhanced male MR can evolve in sym- productive interference evolved, we measured male MR in patry, while counterevidence would support the hypothesis H. titia and two sympatric congeners (Hetaerina occisa, He- (fig. 1). The rubyspot damselfly genus Hetaerina is an ex- taerina americana) across a network of allopatric and sym- ample of a taxon in which reproductive interference occurs patric sites. If male MR were enhanced in sympatry, this at high levels between most but not all sympatric species would imply that male MR evolved via reproductive charac- (Drury et al. 2015a, 2015b). Unlike some other odonates, ter displacement (RCD) and directly contradict the evolu- there is no courtship in Hetaerina; reproductive interac- tionary catch-22 hypothesis (fig. 1). Instead, we find that male tions begin with males clasping females in flight. Building MR does not differ between sympatry and allopatry, which on previous phenotype manipulation experiments and com- suggests that male MR diverged prior to secondary contact parative analyses (Drury et al. 2015a, 2015b), we show here rather than through RCD, supporting the evolutionary that species differences in female wing coloration are predic- catch-22 hypothesis. Pre-speciation Geographic separation (A)(C) Allopatric speciation Correlated divergence Minimal divergence in female phenotypes & in female phenotypes & male mate recognition male mate recognition (B)(D) Secondary contact Low reproductive High reproductive interference interference (E)(F) RCD in female phenotypes Evolutionary & male mate recognition catch-22 Low reproductive High reproductive interference interference Figure 1: Schematic diagram showing two evolutionary routes from speciation in allopatry to low reproductive interference in sympatry. Species either diverge in female phenotypes and male mate recognition in allopatry (A) and are reproductively isolated at the time of sec- ondary contact (B), or they diverge minimally in allopatry (C), experience high levels of reproductive interference on secondary contact (D), and subsequently diverge in female phenotypes and male mate recognition through reproductive character displacement (RCD; E). Alter- natively, species with high reproductive interference might be caught in an evolutionary catch-22 arising from interspecific sexual conflict (F). Evidence for RCD would show that species can escape from high reproductive interference and thereby contradict the catch-22 hypoth- esis, while evidence against RCD would support the catch-22 hypothesis. This content downloaded from 128.097.245.207 on June 27, 2019 12:10:21 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). Catch-22 of Reproductive Interference 000 Methods pendence and the pairwise structure of the data, we com- puted P values using permutation and phylogenetic simu- Male MR and Female Wing Coloration lation methods (appendix, available online; Drury et al. To test the core assumption that similarity in female pheno- 2015b, 2018). types contributes to reproductive interference, we measured male sexual responses to conspecific and heterospecificfe- Testing for RCD in Male MR males at 16 sites in the United States, Mexico, and Costa Rica where two or more species of Hetaerina occur in sympatry To test for RCD of male MR in Hetaerina titia,conspecific (10 species, 13 species pairs) between 2010 and 2017 (ta- and Hetaerina americana females were presented to H. titia ble A1; tables A1–A9 are available online). Following estab- territory holders in sympatry and allopatry,