Advertisement

A novel method to estimate the spatial scale of mate choice in the wild

  • Daniel Estévez
  • Terence P. T. Ng
  • Mónica Fernández-Meirama
  • Jorien M. Voois
  • Antonio Carvajal-Rodríguez
  • Gray A. Williams
  • Juan Galindo
  • Emilio Rolán-AlvarezEmail author
Original Article

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.

Keywords

Echinolittorina malaccana Littorina fabalis Mating preference Assortative mating Disassortative mating Mating preference 

Notes

Acknowledgments

We thank Mary Riádigos for administrative contributions.

Authors’ contribution

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.

Funding information

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.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interests.

Supplementary material

265_2018_2622_Fig5_ESM.png (220 kb)
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)

265_2018_2622_MOESM1_ESM.tif (78 mb)
High resolution image (TIF 79873 kb)
265_2018_2622_MOESM2_ESM.xlsx (15 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)

References

  1. 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 CrossRefGoogle Scholar
  2. Alcock J (2009) Animal behavior: an evolutionary approach. Sinauer Associates, SunderlandGoogle Scholar
  3. Andersson MB (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
  4. 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 CrossRefGoogle Scholar
  5. 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 CrossRefGoogle Scholar
  6. 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 CrossRefPubMedGoogle Scholar
  7. 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 CrossRefGoogle Scholar
  8. 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 CrossRefGoogle Scholar
  9. 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 CrossRefGoogle Scholar
  10. 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
  11. 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 CrossRefPubMedGoogle Scholar
  12. 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 CrossRefGoogle Scholar
  13. 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 CrossRefGoogle Scholar
  14. 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 CrossRefGoogle Scholar
  15. 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 CrossRefGoogle Scholar
  16. 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 CrossRefGoogle Scholar
  17. Edward DA (2015) The description of mate choice. Behav Ecol 26:301–310.  https://doi.org/10.1093/beheco/aru142 CrossRefGoogle Scholar
  18. 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 CrossRefGoogle Scholar
  19. 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 CrossRefGoogle Scholar
  20. Estévez D (2018) Causas del Polimorfismo de Color en Poblaciones Naturales de Littorina fabalis. University of VigoGoogle Scholar
  21. 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 CrossRefGoogle Scholar
  22. 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 CrossRefGoogle Scholar
  23. Fortin M-J, Dale MRT (2005) Spatial analysis: a guide for ecologists. Cambridge University PressGoogle Scholar
  24. Futuyma DJ (2013) Evolution. Sinauer Associates, SunderlandGoogle Scholar
  25. 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 CrossRefGoogle Scholar
  26. Gavrilets S (2004) Fitness landscapes and the origin of species. Princeton University Press, PrincetonGoogle Scholar
  27. Gibson DG (1965) Mating behaviour in Littorina planaxis Philippi (Gastropoda:Prosobranchiata). Veliger 7:134–139Google Scholar
  28. 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 CrossRefGoogle Scholar
  29. 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 CrossRefGoogle Scholar
  30. 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 CrossRefGoogle Scholar
  31. 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 CrossRefGoogle Scholar
  32. 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 CrossRefPubMedGoogle Scholar
  33. 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 CrossRefPubMedGoogle Scholar
  34. Jiang Y, Bolnick DI, Kirkpatrick M (2013) Assortative mating in animals. Am Nat 181:125–138.  https://doi.org/10.1086/670160 CrossRefGoogle Scholar
  35. 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 CrossRefGoogle Scholar
  36. 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 CrossRefGoogle Scholar
  37. Kirkpatrick M, Ryan MJ (1991) The evolution of mating preferences and the paradox of the lek. Nature 350:33–38CrossRefGoogle Scholar
  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 CrossRefPubMedGoogle Scholar
  39. Levin SA (1992) The problem of pattern and scale in ecology. Ecology 73:1943–1967.  https://doi.org/10.2307/1941447 CrossRefGoogle Scholar
  40. 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 CrossRefGoogle Scholar
  41. 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 CrossRefGoogle Scholar
  42. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Ng TPT (2013) Reproductive traits and sexual selection in the mangrove littorinid snails, Littoraria ardouiniana and L. melanostoma. University of Hong KongGoogle Scholar
  44. 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 CrossRefGoogle Scholar
  45. 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 CrossRefGoogle Scholar
  46. 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 CrossRefPubMedGoogle Scholar
  47. 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 CrossRefGoogle Scholar
  48. 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 AcceptedGoogle Scholar
  49. Pielou E (1977) Mathematical ecology. Wiley, New YorkGoogle Scholar
  50. Resetarits WJ, Bernardo J (2001) Experimental ecology: issues and perspectives. Oxford University Press, OxfordGoogle Scholar
  51. 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 CrossRefPubMedGoogle Scholar
  52. 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 CrossRefGoogle Scholar
  53. 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 CrossRefGoogle Scholar
  54. Rosenthal GG (2017) Mate choice: the evolution of sexual decision making from microbes to humans. Princeton University Press, PrincetonGoogle Scholar
  55. 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 CrossRefGoogle Scholar
  56. 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 CrossRefGoogle Scholar
  57. Saur M (1990) Mate discrimination in Littorina littorea (L.) and Littorina saxatilis (Olivi) (Mollusca: Prosobranquia). Hydrobiologia 193:261–270CrossRefGoogle Scholar
  58. 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 CrossRefGoogle Scholar
  59. 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 CrossRefGoogle Scholar
  60. 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 CrossRefGoogle Scholar
  61. 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 CrossRefGoogle Scholar
  62. 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 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Daniel Estévez
    • 1
  • Terence P. T. Ng
    • 2
  • Mónica Fernández-Meirama
    • 1
  • Jorien M. Voois
    • 2
  • Antonio Carvajal-Rodríguez
    • 1
  • Gray A. Williams
    • 2
  • Juan Galindo
    • 1
  • Emilio Rolán-Alvarez
    • 1
    • 3
    Email author return OK on get
  1. 1.Departamento de Bioquímica, Genética e Inmunología, Facultad de BiologíaUniversidad de VigoVigoSpain
  2. 2.The Swire Institute of Marine Science and School of Biological SciencesThe University of Hong KongHong KongChina
  3. 3.Centro de Investigación Mariña da Universidade de Vigo (CIM-UVIGO)VigoSpain

Personalised recommendations