Abstract
Mate choice is a key life history trait and has been widely examined across animal taxa, yet the spatial scale at which animals exercise this choice has rarely been examined. Here we propose a novel method to estimate the spatial scale of mate choice in situ based on a recently developed experimental approach to evaluate, in an unbiased fashion, assortative mating in the wild as a proxy to mate choice. Using mating pairs and the surrounding individuals which were not mating at a particular scale (distance from the mating pair), we correct assortative mating for the known scale-of-choice effect bias due to microgeographical heterogeneity. Appling a linear regression of assortative mating for different scales of correction allows the identification of changes in the scale of choice. In both species, the maximum mate choice │0.35│ occurs at the mating pair position and decreases about 0.35% per cm, which was likely due to the fact that gastropods are slow-moving organisms with limited visual ability, and their mate-searching strategy relies heavily on chemical cues which function over a short distance. The proposed new method can be used to compare species with both positive and negative assortative mating and with mate choice on different traits (e.g. size or colour). As such, we believe that this novel method can be applied to assess the scale of mate choice in other organisms due to the prevalence of assortative mating in the animal kingdom.
Significance statement
Mate choice is a key process in animal evolution, but little is known in relation to the spatial scale at which animals exercise this choice. In several organisms, the choice can be produced by means of visual or vocal cues that can be used by an external observer to study the phenomenon. However, in others, the tactile or olfactory cues are difficult to observe in the wild. We propose a method to detect the strength of assortative mating (as a proxy to mate choice) in the wild. Our method was tested in two snail species, showing that mate choice was exerted at the scale of a few cm, and decreased significantly up to 20 cm from the individual making a choice. The method is beneficial in that it does not require a priori knowledge about the mechanism of mate choice, as it is based on the consequence (i.e. assortative mating) rather than the cause of mate choice, and hence should be applicable to many other species.
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References
Adams SA, Morse DH (2014) Condition-dependent mate choice of a parasitoid wasp in the field. Anim Behav 88:225–232. https://doi.org/10.1016/j.anbehav.2013.12.004
Alcock J (2009) Animal behavior: an evolutionary approach. Sinauer Associates, Sunderland
Andersson MB (1994) Sexual selection. Princeton University Press, Princeton
Arnold SJ, Wade MH (1984) On the measurement of natural and sexual selection: theory. Evolution (N Y) 38(4):709–719. https://doi.org/10.2307/2408383
Atwell A, Wagner WE (2014) Female mate choice plasticity is affected by the interaction between male density and female age in a field cricket. Anim Behav 98:177–183. https://doi.org/10.1016/j.anbehav.2014.10.007
Basolo AL (1998) Evolutionary change in a receiver bias: a comparison of female preference functions. Proc R Soc B 265:2223–2228. https://doi.org/10.1098/rspb.1998.0563
Beltran-Bech S, Richard FJ (2014) Impact of infection on mate choice. Anim Behav 90:159–170. https://doi.org/10.1016/j.anbehav.2014.01.026
Bertorelle G, Bisazza A, Marconato A (1997) Computer simulation suggests that the spatial distribution of males influences female visiting behaviour in the river bullhead. Ethology 103:999–1014. https://doi.org/10.1111/j.1439-0310.1997.tb00142.x
Blyton MDJ, Shaw RE, Peakall R, Lindenmayer DB, Banks SC (2016) The role of relatedness in mate choice by an arboreal marsupial in the presence of fine-scale genetic structure. Behav Ecol Sociobiol 70:313–321. https://doi.org/10.1007/s00265-015-2049-z
Câmara de Aquino J, Joachim-Bravo IS (2014) Relevance of male size to female mate choice in Ceratitis capitata (Diptera: Tephritidae): investigations with wild and laboratory-reared flies. J Insect Behav 27:162–176. https://doi.org/10.1007/s10905-013-9410-8
Candolin U (2003) The use of multiple cues in mate choice. Biol Rev Camb Philos Soc 78:575–595. https://doi.org/10.1017/S1464793103006158
Carvajal-Rodriguez A, Rolán-Alvarez E (2014) A comparative study of Gaussian mating preference functions: a key element of sympatric speciation models. Biol J Linn Soc 113:642–657. https://doi.org/10.1111/bij.12364
Clark HL, Backwell PRY (2015) Temporal and spatial variation in female mating preferences in a fiddler crab. Behav Ecol Sociobiol 69:1779–1784. https://doi.org/10.1007/s00265-015-1990-1
Coyne JA, Elwyn S, Rolán-Alvarez E (2005) Impact of experimental design on Drosophila sexual selection studies: direct effects and comparison to field hybridization data. Evolution (N Y) 59(12):2588. https://doi.org/10.1554/05-454.1
Deb R, Balakrishnan R (2014) The opportunity for sampling: the ecological context of female mate choice. Behav Ecol 25:967–974. https://doi.org/10.1093/beheco/aru072
Dougherty LR, Shuker DM (2015) The effect of experimental design on the measurement of mate choice: a meta-analysis. Behav Ecol 26:311–319. https://doi.org/10.1093/beheco/aru125
Edward DA (2015) The description of mate choice. Behav Ecol 26:301–310. https://doi.org/10.1093/beheco/aru142
Ellis J, Schneider DC (2008) Spatial and temporal scaling in benthic ecology. J Exp Mar Bio Ecol 366:92–98. https://doi.org/10.1016/j.jembe.2008.07.012
Erlandsson J, Kostylev V (1995) Trail following, speed and fractal dimension of movement in a marine prosobranch, Littorina littorea, during a mating and a non-mating season. Mar Biol 122:87–94. https://doi.org/10.1007/BF00349281
Estévez D (2018) Causas del Polimorfismo de Color en Poblaciones Naturales de Littorina fabalis. University of Vigo
Fernández-Meirama M, Carvajal-Rodríguez A, Rolán-Alvarez E (2017a) Testing the role of mating preference in a case of incomplete ecological speciation with gene flow. Biol J Linn Soc 122:549–557. https://doi.org/10.1093/biolinnean/blx107
Fernández-Meirama M, Estévez D, Ng TPT, Williams GA, Carvajal-Rodríguez A, Rolán-Alvarez E (2017b) A novel method for estimating the strength of positive mating preference by similarity in the wild. Ecol Evol 7:11. https://doi.org/10.1002/ece3.2835
Fortin M-J, Dale MRT (2005) Spatial analysis: a guide for ecologists. Cambridge University Press
Futuyma DJ (2013) Evolution. Sinauer Associates, Sunderland
Galipaud M, Bollache L, Wattier R, Dubreuil C, Dechaume-Moncharmont F-X, Lagrue C (2015) Overestimation of the strength of size-assortative pairing in taxa with cryptic diversity: a case of Simpson’s paradox. Anim Behav 102:217–221. https://doi.org/10.1016/j.anbehav.2015.01.032
Gavrilets S (2004) Fitness landscapes and the origin of species. Princeton University Press, Princeton
Gibson DG (1965) Mating behaviour in Littorina planaxis Philippi (Gastropoda:Prosobranchiata). Veliger 7:134–139
Holman L, Kahn AT, Backwell PRY (2014) Fiddlers on the roof: elevation muddles mate choice in fiddler crabs. Behav Ecol 25:271–275. https://doi.org/10.1093/beheco/art125
Holveck MJ, Gauthier AL, Nieberding CM (2015) Dense, small and male-biased cages exacerbate male-male competition and reduce female choosiness in Bicyclus anynana. Anim Behav 104:229–245. https://doi.org/10.1016/j.anbehav.2015.03.025
Hurvich CM, Tsai C-L (1989) Regression and time series model selection in small samples. Biometrika 76:297–307. https://doi.org/10.1093/biomet/76.2.297
Indykiewicz P, Podlaszczuk P, Surmacki A, Kudelska K, Kosicki J, Kamiński M, Minias P (2017) Scale-of-choice effect in the assortative mating by multiple ornamental and non-ornamental characters in the black-headed gull. Behav Ecol Sociobiol 71:183. https://doi.org/10.1007/s00265-017-2411-4
Jennions MD, Petrie M (1997) Variation in mate choice and mating preferences: a review of causes and consequences. Biol Rev Camb Philos Soc 72:283–327. https://doi.org/10.1017/s0006323196005014
Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev Camb Philos Soc 75:21–64. https://doi.org/10.1017/S0006323199005423
Jiang Y, Bolnick DI, Kirkpatrick M (2013) Assortative mating in animals. Am Nat 181:125–138. https://doi.org/10.1086/670160
Johannesson K, Havenhand JN, Jonsson PR, Lindegarth M, Sundin A, Hollander J (2008) Male discrimination of female mucous trails permits assortative mating in a marine snail species. Evolution (N Y) 62:3178–3184. https://doi.org/10.1111/j.1558-5646.2008.00510.x
Johannesson K, Saltin SH, Duranovic I, Havenhand JN, Jonsson PR (2010) Indiscriminate males: mating behaviour of a marine snail compromised by a sexual conflict? PLoS One 5:e1205. https://doi.org/10.1371/journal.pone.0012005
Kirkpatrick M, Ryan MJ (1991) The evolution of mating preferences and the paradox of the lek. Nature 350:33–38
Leroy G (2014) Inbreeding depression in livestock species: review and meta-analysis. Anim Genet 45:618–628. https://doi.org/10.1111/age.12178
Levin SA (1992) The problem of pattern and scale in ecology. Ecology 73:1943–1967. https://doi.org/10.2307/1941447
Mak YM, Williams GA (1999) Littorinids control high intertidal biofilm abundance on tropical, Hong Kong rocky shores. J Exp Mar Bio Ecol 233:81–94. https://doi.org/10.1016/S0022-0981(98)00122-1
Morris MR (1989) Female choice of large males in the treefrog Hyla chrysoscelis: the importance of identifying the scale of choice. Behav Ecol Sociobiol 25(4):275–281. https://doi.org/10.1007/BF00300054
Nandi D, Balakrishnan R (2016) Spatio-temporal dynamics of field cricket calling behaviour: implications for female mate search and mate choice. PLoS One 11:e0165807. https://doi.org/10.1371/journal.pone.0165807
Ng TPT (2013) Reproductive traits and sexual selection in the mangrove littorinid snails, Littoraria ardouiniana and L. melanostoma. University of Hong Kong
Ng TPT, Williams GA (2014) Size-dependent male mate preference and its association with size-assortative mating in a mangrove snail, Littoraria ardouiniana. Ethology 120:995–1002. https://doi.org/10.1111/eth.12271
Ng TP, Williams GA (2015) Penis-rejection in a mangrove littorinid snail: why do females reject males? J Molluscan Stud 81:164–166. https://doi.org/10.1093/mollus/eyu074
Ng TP, Saltin SH, Davies MS, Johannesson K, Stafford R, Williams GA (2013) Snails and their trails: the multiple functions of trail-following in gastropods. Biol Rev Camb Philos Soc 88:683–700. https://doi.org/10.1111/brv.12023
Ng TPT, Williams GA, Davies MS, Stafford R, Rolán-Alvarez E (2016) Sampling scale can cause bias in positive assortative mating estimates: the first evidence in two intertidal snails. Biol J Linn Soc 119:414–419. https://doi.org/10.1111/bij.12839
Ng TPT, Rolán-Alvarez E, Dahlén SS, Davies MS, Estévez D, Stafford R, Williams GA (2018) The causal relationship between sexual selection and sexual size dimorphism in marine gastropods. Anim Behav Accepted
Pielou E (1977) Mathematical ecology. Wiley, New York
Resetarits WJ, Bernardo J (2001) Experimental ecology: issues and perspectives. Oxford University Press, Oxford
Roff DA (2015) The evolution of mate choice: a dialogue between theory and experiment. Ann N Y Acad Sci 1360:1–15. https://doi.org/10.1111/nyas.12743
Rolán-Alvarez E, Caballero A (2000) Estimating sexual selection and sexual isolation effects from mating frequencies. Evolution (N Y) 54:30–36. https://doi.org/10.1111/j.0014-3820.2000.tb00004.x
Rolán-Alvarez E, Carvajal-Rodríguez A, de Coo A, Cortés B, Estévez D, Ferreira M, González R, Briscoe AD (2015) The scale-of-choice effect and how estimates of assortative mating in the wild can be biased due to heterogeneous samples. Evolution (N Y) 69:1845–1857. https://doi.org/10.1111/evo.12691
Rosenthal GG (2017) Mate choice: the evolution of sexual decision making from microbes to humans. Princeton University Press, Princeton
Sale PF (1998) Appropriate spatial scales for studies of reef-fish ecology. Aust J Ecol 23:202–208. https://doi.org/10.1111/j.1442-9993.1998.tb00721.x
Saltin SH, Schade H, Johannesson K (2013) Preference of males for large females causes a partial mating barrier between a large and a small ecotype of Littorina fabalis (W. Turton, 1825). J Molluscan Stud 79:128–132. https://doi.org/10.1093/mollus/eyt003
Saur M (1990) Mate discrimination in Littorina littorea (L.) and Littorina saxatilis (Olivi) (Mollusca: Prosobranquia). Hydrobiologia 193:261–270
Taborsky B, Guyer L, Taborsky M (2009) Size-assortative mating in the absence of mate choice. Anim Behav 77(2):439–448. https://doi.org/10.1016/j.anbehav.2008.10.020
Turner MG, O’Neill RV, Gardner RH, Milne BT (1989) Effects of changing spatial scale on the analysis of landscape pattern. Landsc Ecol 3:153–162. https://doi.org/10.1007/BF00131534
Vasudev D, Fletcher RJ (2016) Mate choice interacts with movement limitations to influence effective dispersal. Ecol Model 327:65–73. https://doi.org/10.1016/j.ecolmodel.2016.01.014
Witte K, Kureck IM (2015) Mate-choice copying: status quo and where to go. Curr Zool 61:1073–1081. https://doi.org/10.1093/czoolo/61.6.1073
Zahradnik TD, Lemay MA, Boulding EG (2008) Choosy males in a littorinid gastropod: male Littorina subrotundata prefer large and virgin females. J Molluscan Stud 74:245–251. https://doi.org/10.1093/mollus/eyn014
Acknowledgments
We thank Mary Riádigos for administrative contributions.
Funding
This work was supported by the Xunta de Galicia (Axudas do programa de consolidación e estruturación de unidades de investigacións competitivas do SUG; ED431C 2016-037), FONDOS FEDER (‘unha maneira de facer europa’) and the Ministerio de Economía y Competitividad (CGL2016-75482-P). The study was also partly funded by the Research Grants Council of the Hong Kong SAR Government via the General Research Fund (GRF) (grant no.: HKU 17121914 M) to G.A.W.
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DE performed sampling, dissection and analyses on Littorina fabalis; TPTN and JMV performed sampling, dissection and analyses on Echinolittorina malaccana; MF-M performed modelling on Echinolittorina data; JMV performed size measurements on Echinolittorina; AC-R performed modelling on Littorina; GAW performed sampling on Echinolittorina; JG performed sampling on Littorina fabalis; and ER-A performed sampling in both species, analyzed output data and wrote the first MS draft. All authors contributed substantially to revision and discussion.
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Supplementary Figure S1
Comparison of Assortative mating estimates and SCE corrections by using weighted or unweighted means of IPSI (Littorina fabalis) or Pearson’s r (Ecchinolittorina malacana). As it can be observed, trends in both graphs of each estimate do not change substantially if using unweighted means. Error bars represent the SE and are greater in unweighted estimates. (PNG 220 kb)
ESM 2
Supplementary Table S1. The scale of the captured unmated specimens (used to correct the assortative mating estimate) is regressed against the dependent variable SCE (which allow the pooling of different data sets). Four alternative regression models (linear, logarithmic, inverse, quadratic) are compared by the ACAIC criterion. Species and samples as in M&M. N is number of points in the regression. The inverse regression models showed always the smaller value and is therefore the chosen model for the rest of the analysis. Supplementary Table S2. The inverse regression model applied on the different data sets using the parametric (black ink) and bootstrap (blue ink) framework, to show the coincidence in parameter estimation and significance. The statistics r2, a and b represent, correspondingly, the proportion of variance explained, constant and slope in the regressions. (XLSX 15 kb)
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Estévez, D., Ng, T.P.T., Fernández-Meirama, M. et al. A novel method to estimate the spatial scale of mate choice in the wild. Behav Ecol Sociobiol 72, 195 (2018). https://doi.org/10.1007/s00265-018-2622-3
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DOI: https://doi.org/10.1007/s00265-018-2622-3