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Influence of Female Cuticular Hydrocarbon (CHC) Profile on Male Courtship Behavior in Two Hybridizing Field Crickets Gryllus

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Influence of Female Cuticular Hydrocarbon (CHC) Profile on Male Courtship Behavior in Two Hybridizing Field Crickets Gryllus Heggeseth et al. BMC Evolutionary Biology (2020) 20:21 https://doi.org/10.1186/s12862-020-1587-9 RESEARCH ARTICLE Open Access Influence of female cuticular hydrocarbon (CHC) profile on male courtship behavior in two hybridizing field crickets Gryllus firmus and Gryllus pennsylvanicus Brianna Heggeseth1,2, Danielle Sim3, Laura Partida3 and Luana S. Maroja3* Abstract Background: The hybridizing field crickets, Gryllus firmus and Gryllus pennsylvanicus have several barriers that prevent gene flow between species. The behavioral pre-zygotic mating barrier, where males court conspecifics more intensely than heterospecifics, is important because by acting earlier in the life cycle it has the potential to prevent a larger fraction of hybridization. The mechanism behind such male mate preference is unknown. Here we investigate if the female cuticular hydrocarbon (CHC) profile could be the signal behind male courtship. Results: While males of the two species display nearly identical CHC profiles, females have different, albeit overlapping profiles and some females (between 15 and 45%) of both species display a male-like profile distinct from profiles of typical females. We classified CHC females profile into three categories: G. firmus-like (F; including mainly G. firmus females), G. pennsylvanicus-like (P; including mainly G. pennsylvanicus females), and male-like (ML; including females of both species). Gryllus firmus males courted ML and F females more often and faster than they courted P females (p < 0.05). Gryllus pennsylvanicus males were slower to court than G. firmus males, but courted ML females more often (p < 0.05) than their own conspecific P females (no difference between P and F). Both males courted heterospecific ML females more often than other heterospecific females (p < 0.05, significant only for G. firmus males). Conclusions: Our results suggest that male mate preference is at least partially informed by female CHC profile and that ML females elicit high courtship behavior in both species. Since ML females exist in both species and are preferred over other heterospecific females, it is likely that this female type is responsible for most hybrid offspring production. Keywords: Mate choice, Hybrid zone, Pre-mating barrier, Speciation, Introgression Background exhibit differential courtship behavior to females based on To fully understand mate choice and its influence on speci- varioustraitssuchassize[4, 16, 22], relatedness [6, 35, 56] ation, we need to understand the mechanisms behind this and species membership [25, 38, 44]. choice. Mate choice in the form of preference for conspe- The morphologically and behaviorally similar hybridizing cifics is a pre-zygotic barrier that prevents gene flow be- field crickets, Gryllus firmus [53]andGryllus pennsylvanicus tween species and is important because by acting early in [19], provide an opportunity to better understand the role of the life cycle, it can prevent more gene flow than other later male mate preferences in reproductive isolation. These two acting barriers [10].Whilematechoicehastraditionally species form a well-described mosaic hybrid zone [20, 30, been almost synonymous with female mate choice [28], 48] and have several barriers that limit gene exchange [14, male mate choice, or preference, has now been reported 19, 31, 37]. Their pre-mating barrier is largely explained by even in species with little male parental care [15]. Males differential male courtship; males court conspecific females more readily and intensely than they court heterospecifics [38]. Therefore, while female crickets ultimately decide * Correspondence: [email protected] 3Department of Biology, Williams College, Williamstown, MA, USA whether or not to mate (as they have to mount the male), Full list of author information is available at the end of the article © The Author(s). 2020 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Heggeseth et al. BMC Evolutionary Biology (2020) 20:21 Page 2 of 9 male courtship intensity plays a significant role in their deci- that males of both species mate with heterospecific ML sion and females often mate with intensely courting males (male-like) females at a higher rate than other heterospe- andwillnevermateanon-courtingmale[38]. cifics, suggesting that males can indeed detect and use While barriers to gene exchange are well described in CHC information for courtship decisions. Therefore, it these crickets, the mechanism behind this male mate is possible that ML (male-like) females produce most of preference is not understood. While morphological dif- the hybrid offspring in the hybrid zone. ferences are often used in mate recognition, this is un- like to be the case between the morphologically similar Results G. firmus and G. pennsylvanicus which might instead Cuticular hydrocarbon analysis use chemical signals such as cuticular hydrocarbons For the gas chromatography analysis, we used the similar (CHCs). These compounds serve as contact pheromones methods of Maroja et al. [38], we scored 17 peaks (Table 1) to a wide variety of insects [2, 11, 12, 17, 33, 34, 50], are in 259 individuals (GP♂: n =67,GP♀: n =65,GF♂: n = 68, sexually dimorphic in many species [8, 9, 24, 59], includ- GF♀: n = 59). Males typically have fewer peaks than females ing field crickets [38, 42, 61–64, 67], and are used for mate with less variation between individuals (Table 1). Size (GP♂ choice in various insect species [23, 45, 54, 59, 60]. In G. 5.67 ± 0.47 cm, GP♀:5.90 ± 0.30 cm, GF♂: 5.42 ± 0.42 cm, firmus and G. pennsylvanicus CHC composition is differ- GF♀: 5.76 ± 0.34 cm) was significantly different between ent between sexes however, while males of both species sexes (F1, 249 =35.0, p < 0.001) and between species (F1, share the same composition, females of the two species 249 = 16.6, p < 0.001), but there is no significant interaction are different but overlapping [38]. Furthermore, a subset between sex and species (F1, 249 =1.4, p = 0.24) in a two- of females from both species (between 15 and 45% based wayANOVA,however,unlikepreviousstudies,G. pennsyl- on this and previous data) exhibits a pattern that is typical vanicus were the larger species in our sample [30]. of that of a male (male-like females, ML), the relevance of As reported before [38], the first two principal compo- this pattern is unknown. This female CHC profile variabil- nents of relative CHC peak proportion (percent of each ity, with both unique and shared patterns between species, peak) and composition (presence or absence of peak) were suggests that it could be the mechanism behind male mate less varied within males of both species with the area of the recognition and could thus explain why males sometimes, convex hull for males equal to 4.8 and 25.3 as compared to but not always, court heterospecifics. 46.6 and 38.8 for females, for peak proportion and compos- Our goal is to test the hypothesis that female CHC ition respectively (Fig. 1). Moreover, while females had profile informs male mate preferences in the hybridizing significantly different CHC profiles between species [38], field crickets G. firmus and G. pennsylvanicus. We show some of the profiles were overlapping between species and Table 1 Average relative proportion and standard deviation of the 17 scored peaks for CHC analysis PEAKS GP ♂ (n = 67) GP ♀ (n = 65) GF ♂(n = 68) GF ♀ (n = 59) Mean SD % zero Mean SD % zero Mean SD % zero Mean SD % zero F0 0.00 0.00 100.00 10.28 12.61 8.96 0.00 0.00 100.00 0.17 0.38 77.97 F4 0.02 0.06 89.55 1.16 1.16 14.93 0.24 0.42 48.53 1.47 1.40 22.03 M0 2.78 1.37 2.99 17.36 13.22 1.49 2.38 1.38 0.00 4.62 3.79 10.17 F5 0.00 0.00 100.00 7.84 9.55 23.88 0.00 0.00 100.00 2.84 3.54 25.42 M1 8.53 4.10 2.99 7.69 4.66 0.00 8.33 5.17 0.00 6.79 3.68 1.69 F8 1.37 0.85 4.48 3.37 2.94 1.49 1.10 0.73 4.41 3.02 1.89 5.08 M3 4.25 3.36 14.93 2.77 2.04 13.43 6.48 4.18 14.71 5.03 2.82 3.39 M4 17.81 17.07 38.81 14.30 14.98 31.34 24.01 15.63 19.12 6.44 9.96 37.29 M5 33.86 16.50 10.45 10.65 11.06 4.48 25.87 12.26 7.35 6.93 8.89 16.95 M6 16.66 9.26 7.46 10.85 4.14 0.00 15.38 7.35 1.47 19.12 7.73 3.39 F10 0.02 0.08 92.54 3.44 4.15 16.42 0.04 0.14 91.18 8.93 6.46 3.39 M7 8.03 8.12 38.81 4.42 4.56 34.33 9.08 6.49 22.06 11.37 5.31 1.69 F11 0.00 0.00 100.00 0.20 0.59 70.15 0.03 0.09 91.18 1.21 0.93 20.34 F12 0.35 1.95 74.63 0.85 1.37 35.82 1.55 1.48 13.24 8.18 9.22 3.39 M8 6.28 8.14 38.81 3.20 4.49 40.30 5.28 5.76 42.65 2.61 3.64 49.15 F13 0.04 0.26 97.01 1.47 3.51 44.78 0.01 0.07 95.59 6.73 6.30 18.64 F14 0.00 0.00 100.00 0.16 0.49 85.07 0.22 0.81 86.76 4.54 3.52 10.17 Heggeseth et al.
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