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Opposing Dominance Within a Color Gene Block Is Associated with Maladaptive Hybrid Signal Discordance

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Opposing Dominance Within a Color Gene Block Is Associated with Maladaptive Hybrid Signal Discordance bioRxiv preprint doi: https://doi.org/10.1101/2021.02.18.431741; this version posted February 18, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. de Zwaan et al., 17 Feb 2021 – preprint copy - BioRxiv Opposing dominance within a color gene block is associated with maladaptive hybrid signal discordance Devin R. de Zwaan1, Jacqueline Mackenzie2, Else Mikklesen2, and Silu Wang2,3* 1 Department of Forest and Conservation Sciences, 2424 Main Mall, University of British Columbia, BC, V6T1Z4, Canada 2 Department of Zoology, 6270 University Blvd, University of British Columbia, BC, Vancouver, BC, V6T1Z4, Canada 3 Current address: Department of Integrative Biology, University of California, Berkeley * Correspondence: [email protected] Abstract Color divergence is increasingly recognized as important for speciation in songbirds through its influence on social dynamics. However, the behavioral mechanisms underlying the eco-evolutionary feedback that acts across species boundaries is poorly understood. The hybrid zone between Setophaga occidentalis (SOCC) and S. townsendi (STOW) in the Cascade mountain ranges provides a natural observatory to test the interplay between genetics and social behaviour in maintaining species boundaries. Recently, we found that selection within a gene block underpinning color variation (ASIP-RALY) has maintained a stable and narrow hybrid zone. Here we investigated the social signaling roles of cheek darkness and flank streaking, two color traits linked to ASIP-RALY that reflect opposing dominance of SOCC and STOW alleles. We found that both traits act as honest badges of status, as they predicted male breeding quality. The opposing dominance effects of ASIP-RALY resulted in signal discordance for heterozygotes, which in turn was associated with inferior hybrid territorial performance, a fitness proxy quantified by vocal and physical responses of resident males to a decoy intruder. Taken together, this study highlights a potential behavioral mechanism underlying selection acting on a simple genetic architecture that has maintained a stable species boundary over decades despite significant gene flow. Keywords: speciation, ASIP, RALY, color genes, badge of status, hybrid fitness, honest signal, territoriality, Setophaga. Introduction secondary contact, divergent systems may lead to signal interference and Bird plumage is often characterized by distinct patches of compromised territorial performance among hybrid individuals with pigments (e.g., carotenoids, melanins) where the patch size or color discordant badges (Birch 1957; Schultz and Switzer 2001; Gröning and intensity can relay information about an individual’s genetic or Hochkirch 2008). Incompatible badges of status within hybrids may thus phenotypic quality, including ‘good genes’, nutritional state, incur reduced hybrid fitness. Badges of status and their genetic basis are immunocompetence, parental investment, or territorial dominance often investigated within species or populations, but rarely across species (McGraw and Ardia 2003; Hill 2006; Searcy and Nowicki 2010; boundaries. Here we assessed multiple badges of status within allopatric Svensson and Wong 2011). In the context of a social environment, and hybrid zone populations of two closely related wood-warbler species, ‘badges of status’ may signal social dominance as a mechanism to limit Setophaga townsendi and Setophaga occidentalis, to understand the costly combats among territorial individuals (Rohwer 1975; Studd and potential role of plumage traits and social dominance in speciation. Robertson 1985). Social dominance can be costly due to detrimental Divergent badges of status may be involved in speciation levels of testosterone along with frequent energy- and time-demanding between S. townsendi (hereafter abbreviated as ‘STOW’) and S. territorial challenges (Goymann and Wingfield 2004). Therefore, badges occidentalis (‘SOCC’) due to frequent heterospecific male competitions of status are thought to emerge and be maintained in populations (Pearson and Rohwer 2000) within the narrow hybrid zone along the characterized by individuals that vary in their ability to overcome these Cascade mountain range (Rohwer and Wood 1998; Wang et al. 2019, costs (i.e., body condition, aggression), as well as repeated territorial 2020b). Recent evidence revealed that the key genomic differentiation contests for mates and limited resources (1,2). To be considered an between allopatric parental populations resides within a color gene block, ‘honest’ signal, plumage badges should be variable among counterparts ASIP-RALY, which pleiotropically underpins variation in multiple color of the same sex, correlate with quality or combat ability of the carrier traits among hybrids sampled in the hybrid zone; particularly the extent (Rohwer 1975, 1982; Rohwer and Rohwer 1978), and be a component of of black pigmentation (melanin) and yellow (carotenoid) coloration in the aggressive interactions among counterparts, either by dissuading combat crown, cheek, breast, and flank, all of which are diagnostic for the two among individuals of different status or triggering combats between species (Wang et al. 2020b). Spatiotemporal analysis of ASIP-RALY individuals with similar badges (Rohwer 1975). Support for honest allele frequency revealed selection acting on this gene block (Wang et al. badges of status is often context dependent, but there is ample 2020b), although the mechanism of selection remained unclear. observational and experimental evidence to suggest that this mechanism One potential mechanism underlying selection against of territorial signaling is widespread (e.g., (Studd and Robertson 1985; individuals heterozygous for ASIP-RALY genotypes could be reduced Møller 1987; Safran et al. 2008; Hund et al. 2020). hybrid fitness through incompatible badges of status, or the breakdown Badges of status may be divergent among closely-related of signal reliability (Vortman et al. 2011, 2013). Species-specific species (Rohwer 1982) and thus a potentially important component of carotenoid and melanic color features likely serve as badges of status in speciation. When badges established in isolated populations come into this system, as they vary in intensity within species (Jackson et al. 1992; 1 bioRxiv preprint doi: https://doi.org/10.1101/2021.02.18.431741; this version posted February 18, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. de Zwaan et al., 17 Feb 2021 – preprint copy - BioRxiv Wang et al. 2020b) and are involved in male-male competition (Pearson Badges of status 2000; Pearson et al. 2000). Two of these ASIP-RALY-associated traits, To test whether flank streaking and cheek coloration may act flank streaking and cheek darkening, demonstrated opposing dominance: as badges of status or signal individual quality, we conducted linear the STOW allele is dominant in flank streaking, whereas the SOCC allele regression of breeding condition PC1 against each of the plumage is dominant in cheek darkening (Wang et al. 2020b). Based on this variables accounting for population (parental STOW, SOCC, or hybrid pleiotropic opposing dominance effect of ASIP-RALY gene block, we zone): predicted discordant cheek and flank ancestry in heterozygous individuals. If cheek darkening and flank streaking act as honest signals lm (condition = plumage ´ population) [1] within species and are divergent between species, individuals with discordant badges of status may disproportionately suffer the costs of A significant slope would indicate that these plumage traits are associated territorial disputes, resulting in reduced social dominance and fitness. with individual condition within populations and therefore have the We investigated the mechanism underlying selection on the potential to act as badges of status. A significant interaction term would ASIP-RALY gene block that may maintain or reinforce the STOW- indicate divergence in signal honesty among populations. SOCC species boundary by addressing three questions: (1) Do cheek and flank plumage patches act as badges of status within Color genotype species and diverge between species? (2) Does the pleiotropic opposing dominance effect of ASIP-RALY lead Genotype data was acquired from our previous study (Wang et to discordance of badges of status in the hybrid zone? al. 2020b), in which the genotypes of color gene block ASIP-RALY was (3) Are hybrid individuals with discordant badges of status characterized denoted as OO, OT, TT for homozygous SOCC, heterozygous, and by reduced territorial performance? homozygous STOW, respectively. Dominance coefficients for each plumage trait were determined by the following equation: Materials and Methods ℎ = (�̅"" − �!"̅ )/(�̅"" − �!!̅ ) [2] Study site ̅ ̅ ̅ We carried out this study in the hybrid zone within the where �!!, �!", and �"" are mean phenotype individuals with OO, OT, Cascades mountain range of Washington as described in our previous and TT ASIP-RALY genotype. The STOW allele is dominant if h = 0, study (Wang et al. 2019). Detailed sampling information is summarized whereas the SOCC allele is dominant if h = 1. The bootstrap distribution
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