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Animal Cognition

, Volume 22, Issue 6, pp 1085–1094 | Cite as

Female cognitive performance and mass are correlated with different aspects of mate choice in the zebra finch (Taeniopygia guttata)

  • C. HowellEmail author
  • R. Anderson
  • E. P. Derryberry
Original Paper

Abstract

A female’s cognitive ability may influence her mate preferences through various mechanisms. These mechanisms include the direct effect of cognitive ability on the information-processing skills used during mate choice, and the indirect effect of cognitive ability on quality when females mate assortatively. Here, we examined whether the ability to learn a novel foraging task, a cognitive skill which has been associated with reproductive success in other capacities, was correlated with song preferences in female zebra finches (Taeniopygia guttata). Female preferences were measured in an operant testing chamber where hops on a perch triggered song playback. Females were given the choice of (1) conspecific vs. heterospecific song and (2) high-quality male vs. low-quality male conspecific song. We found that female performance on the novel foraging task was positively correlated with preference for conspecific song, but not with preference for high-quality male song. Instead, female mass was positively correlated with preference for high-quality male song, potentially signifying that female mass is a stronger predictor of female quality in assortative mating than female cognitive performance. Female mass and cognitive performance were unrelated. Our results suggest that the particular traits of a female that affect conspecific preference do not necessarily affect preference for high-quality males.

Keywords

Sexual selection Assortative mating Cognitive ability Conspecific preference Female choice Mate choice Zebra finch Taeniopygia guttata 

Notes

Acknowledgements

We thank K. Micotto and M. Daoud for contributing to data collection. We thank J. Danner for Rufous-collared sparrow recordings. We thank S. Lipshutz, M. Berlow, C. Coomes, and M. Blum for comments on earlier versions of this manuscript.

Funding

This work was supported by the Tulane Neuroscience Program (to CH) and the National Science Foundation (IOS-1354756 to EPD).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

All procedures performed in studies involving animals were in accordance with the ethical standards of the Tulane Animal Care and Use Committee, Protocol 0427R.

Supplementary material

10071_2019_1299_MOESM1_ESM.docx (111 kb)
Supplementary material 1 (DOCX 111 kb)

References

  1. Anderson RC, Peters S, Nowicki S (2014) Effects of early auditory experience on the development of local song preference in female swamp sparrows. Behav Ecol Sociobiol 68:437–447.  https://doi.org/10.1007/s00265-013-1658-7 CrossRefGoogle Scholar
  2. Anderson RC, Searcy WA, Peters S, Hughes M, DuBois AL, Nowicki S (2017) Song learning and cognitive ability are not consistently related in a songbird. Anim Cogn 20:309–320.  https://doi.org/10.1007/s10071-016-1053-7 CrossRefPubMedGoogle Scholar
  3. Andersson M (1994) Sexual Selection. In: Krebs JR, Clutton-Brock TH (eds) Monographs in behavior and ecology. Princeton University Press, PrincetonGoogle Scholar
  4. Ashton BJ, Ridley AR, Edwards EK, Thornton A (2018) Cognitive performance is linked to group size and affects fitness in Australian magpies. Nature 554:364–367.  https://doi.org/10.1038/nature25503 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Audet J-N, Lefebvre L (2017) What’s flexible in behavioral flexibility? Behav Ecol 00:1–5.  https://doi.org/10.1093/beheco/arx007 CrossRefGoogle Scholar
  6. Bailey NW (2011) Mate choice plasticity in the field cricket Teleogryllus oceanicus: effects of social experience in multiple modalities. Behav Ecol Sociobiol 65:2269–2278.  https://doi.org/10.1007/s00265-011-1237-8 CrossRefGoogle Scholar
  7. Bakker T, Kunzler R, Mazzi D (1999) Condition-related mate choice in sticklebacks. Nature 401:255–257CrossRefGoogle Scholar
  8. Basolo AL (2004) Variation between and within the sexes in body size preferences. Anim Behav 68:75–82.  https://doi.org/10.1016/j.anbehav.2003.07.019 CrossRefGoogle Scholar
  9. Bates D, Mächler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48.  https://doi.org/10.18637/jss.v067.i01 CrossRefGoogle Scholar
  10. Bateson M, Healy SD (2005) Comparative evaluation and its implications for mate choice. Trends Ecol Evol 20:659–664.  https://doi.org/10.1016/j.tree.2005.08.013 CrossRefPubMedGoogle Scholar
  11. Bel-Venner MC, Dray S, Allainé D, Menu F, Venner S (2008) Unexpected male choosiness for mates in a spider. Proc R Soc B Biol Sci 275:77–82.  https://doi.org/10.1098/rspb.2007.1278 CrossRefGoogle Scholar
  12. Boogert NJ, Giraldeau LA, Lefebvre L (2008) Song complexity correlates with learning ability in zebra finch males. Anim Behav 76:1735–1741.  https://doi.org/10.1016/j.anbehav.2008.08.009 CrossRefGoogle Scholar
  13. Boogert NJ, Anderson RC, Peters S, Searcy WA, Nowicki S (2011) Song repertoire size in male song sparrows correlates with detour reaching, but not with other cognitive measures. Anim Behav 81:1209–1216.  https://doi.org/10.1016/j.anbehav.2011.03.004 CrossRefGoogle Scholar
  14. Bouchard J, Goodyer W, Lefebvre L (2007) Social learning and innovation are positively correlated in pigeons (Columba livia). Anim Cogn 10:259–266.  https://doi.org/10.1007/s10071-006-0064-1 CrossRefPubMedGoogle Scholar
  15. Buchanan KL, Spencer KA, Goldsmith AR, Catchpole CK (2003) Song as an honest signal of past developmental stress in the European starling (Sturnus vulgaris). Proc R Soc London 270:1149–1156.  https://doi.org/10.1016/S0018-506X(03)00124-7 CrossRefGoogle Scholar
  16. Burley NT, Foster VS (2006) Variation in female choice of mates: condition influences selectivity. Anim Behav 72:713–719.  https://doi.org/10.1016/j.anbehav.2006.01.017 CrossRefGoogle Scholar
  17. Burley NT, Hamedani E, Symanski C (2018) Mate choice decision rules: trait synergisms and preference shifts. Ecol Evol 8:2380–2394.  https://doi.org/10.1002/ece3.3831 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Byers JA, Byers AA, Dunn SJ (2006) A dry summer diminishes mate search effort by pronghorn females: evidence for a significant cost of mate search. Ethology 112:74–80.  https://doi.org/10.1111/j.1439-0310.2006.01127.x CrossRefGoogle Scholar
  19. Catchpole CK, Slater PJB (2008) Bird song: biological themes and variations, 2nd edn. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  20. Cauchard L, Boogert NJ, Lefebvre L, Dubois F, Doligez B (2013) Problem-solving performance is correlated with reproductive success in a wild bird population. Anim Behav 85:19–26.  https://doi.org/10.1016/j.anbehav.2012.10.005 CrossRefGoogle Scholar
  21. Chantal V, Gibelli J, Dubois F (2016) Male foraging efficiency, but not male problem-solving performance, influences female mating preferences in zebra finches. PeerJ 4:e2409.  https://doi.org/10.7717/peerj.2409 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Chen J, Zou Y, Sun Y-H, Ten Cate C (2019) Problem-solving males become more attractive to female budgerigars. Science 363:166–167.  https://doi.org/10.1126/science.aau8181 CrossRefPubMedGoogle Scholar
  23. Clayton NS (1990a) Assortative mating in zebra finch subspecies, Taeniopygia guttata guttata and T. g. castanotis. Philos Trans R Soc London B.  https://doi.org/10.1098/rstb.1990.0205 CrossRefGoogle Scholar
  24. Clayton NS (1990b) The effects of cross-fostering on assortative mating between zebra finch subspecies. Anim Behav.  https://doi.org/10.1016/s0003-3472(05)80176-9 CrossRefGoogle Scholar
  25. Cole EF, Morand-Ferron J, Hinks AE, Quinn JL (2012) Cognitive ability influences reproductive life history variation in the wild. Curr Biol 22:1808–1812.  https://doi.org/10.1016/j.cub.2012.07.051 CrossRefPubMedGoogle Scholar
  26. Corral-López A, Bloch NI, Kotrschal A, Van Der Bijl W, Buechel SD, Mank JE, Kolm N (2017) Female brain size affects the assessment of male attractiveness during mate choice. Sci Adv 3:1–9.  https://doi.org/10.1126/sciadv.1601990 CrossRefGoogle Scholar
  27. Dougherty LR, Guillette LM (2018) Linking personality and cognition: a meta-analysis. Philos Trans R Soc B Biol Sci 373:20170282.  https://doi.org/10.1098/rstb.2017.0282 CrossRefGoogle Scholar
  28. DuBois AL, Nowicki S, Peters S, Rivera-Cáceres KD, Searcy WA (2018) Song is not a reliable signal of general cognitive ability in a songbird. Anim Behav 137:205–213.  https://doi.org/10.1016/j.anbehav.2018.01.020 CrossRefGoogle Scholar
  29. Farrell TM, Neuert MAC, Cui A, MacDougall-Shackleton SA (2015) Developmental stress impairs a female songbird’s behavioural and neural response to a sexually selected signal. Anim Behav 102:157–167.  https://doi.org/10.1016/j.anbehav.2015.01.018 CrossRefGoogle Scholar
  30. Farrell TM, Morgan A, MacDougall-Shackleton SA (2016) Developmental stress impairs performance on an association task in male and female songbirds, but impairs auditory learning in females only. Anim Cogn 19:1–14.  https://doi.org/10.1007/s10071-015-0908-7 CrossRefPubMedGoogle Scholar
  31. Fawcett TW, Johnstone RA (2003) Mate choice in the face of costly competition. Behav Ecol 14:771–779.  https://doi.org/10.1093/beheco/arg075 CrossRefGoogle Scholar
  32. Fisher MO, Nager RG, Monaghan P (2006) Compensatory growth impairs adult cognitive performance. PLoS Biol 4:1462–1466.  https://doi.org/10.1371/journal.pbio.0040251 CrossRefGoogle Scholar
  33. Griffin AS, Guez D (2014) Innovation and problem solving: a review of common mechanisms. Behav Processes 109:121–134.  https://doi.org/10.1016/j.beproc.2014.08.027 CrossRefPubMedGoogle Scholar
  34. Griffin AS, Guillette LM, Healy SD (2015) Cognition and personality: an analysis of an emerging field. Trends Ecol Evol 30:207–214.  https://doi.org/10.1016/j.tree.2015.01.012 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Griggio M, Hoi H (2010) Only females in poor condition display a clear preference and prefer males with an average badge. BMC Evol Biol 10:261.  https://doi.org/10.1186/1471-2148-10-261 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Härdling R, Kokko H (2005) The evolution of prudent choice. Evol Ecol Res 7:697–715.  https://doi.org/10.1046/j.1461-0248.1999.00075.x CrossRefGoogle Scholar
  37. Holveck M-J, Riebel K (2010) Low-quality females prefer low-quality males when choosing a mate. Proc R Soc B Published 277:153–160.  https://doi.org/10.1098/rspb.2009.1222 CrossRefGoogle Scholar
  38. Holveck M-J, Riebel K (2014) Female zebra finches learn to prefer more than one song and from more than one tutor. Anim Behav 88:125–135.  https://doi.org/10.1016/j.anbehav.2013.11.023 CrossRefGoogle Scholar
  39. Holveck MJ, Geberzahn N, Riebel K (2011) An experimental test of condition-dependent male and female mate choice in zebra finches. PLoS One 6(8):e23974.  https://doi.org/10.1371/journal.pone.0023974 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Hunt J, Brooks R, Jennions MD (2005) Female mate choice as a condition-dependent life-history trait. Am Nat 166:79–92.  https://doi.org/10.1086/430672 CrossRefPubMedGoogle Scholar
  41. 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
  42. Johnson JB, Basolo AL (2003) Predator exposure alters female mate choice in the green swordtail. Behav Ecol 14:619–625.  https://doi.org/10.1093/beheco/arg046 CrossRefGoogle Scholar
  43. Kitaysky AS, Kitaiskaia EV, Piatt JF, Wingfield JC (2006) A mechanistic link between chick diet and decline in seabirds? Proc R Soc B Biol Sci 273:445–450.  https://doi.org/10.1098/rspb.2005.3351 CrossRefGoogle Scholar
  44. Kriengwatana B, MacDougall-Shackleton SA, Farrell TM, Garcia L, Aitken SDT (2015) Early-life nutritional stress affects associative learning and spatial memory but not performance on a novel object test. Behaviour 152:195–218.  https://doi.org/10.1163/1568539X-00003239 CrossRefGoogle Scholar
  45. Lynch KS, Rand AS, Ryan MJ, Wilczynski W (2005) Plasticity in female mate choice associated with changing reproductive states. Anim Behav 69:689–699.  https://doi.org/10.1016/j.anbehav.2004.05.016 CrossRefGoogle Scholar
  46. Mendelson TC, Shaw KL (2012) The (mis)concept of species recognition. Trends Ecol Evol 27(8):421–427.  https://doi.org/10.1016/j.tree.2012.04.001 CrossRefPubMedGoogle Scholar
  47. Nowicki S, Searcy WA, Peters S (2002) Brain development, song learning and mate choice in birds: a review and experimental test of the “nutritional stress hypothesis”. J Comp Physiol A 188:1003–1014.  https://doi.org/10.1007/s00359-002-0361-3 CrossRefGoogle Scholar
  48. Nuechterlein GL, Buitron D (1998) Interspecific mate choice by late-courting male western grebes. Behav Ecol 9:313–321CrossRefGoogle Scholar
  49. Pfennig KS (2007) Facultative mate choice drives hybridization. Science (80-) 318:965–967.  https://doi.org/10.1126/science.1146035 CrossRefGoogle Scholar
  50. Prather JF, Nowicki S, Anderson RC, Peters S, Mooney R (2009) Neural correlates of categorical perception in learned vocal communication. Nat Neurosci 12:221–228.  https://doi.org/10.1038/nn.2246 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Pravosudov VV, Lavenex P, Omanska A (2005) Nutritional deficits during early development affect hippocampal structure and spatial memory later in life. Behav Neurosci 119:1368–1374.  https://doi.org/10.1037/0735-7044.119.5.1368 CrossRefPubMedGoogle Scholar
  52. R Development Core Team (2016) R: a language and environment for statistical computing. R Found Stat Comput Vienna Austria. 0:{ISBN} 3-900051-07-0.  https://doi.org/10.1038/sj.hdy.6800737 CrossRefGoogle Scholar
  53. Riebel K (2009a) Chapter 6 song and female mate choice in zebra finches: a review. Adv Study Behav 40:197–238.  https://doi.org/10.1016/s0065-3454(09)40006-8 CrossRefGoogle Scholar
  54. Riebel K (2009b) Song and female mate choice in zebra finches: a review, 1st edn. Elsevier Inc, AmsterdamGoogle Scholar
  55. Rowe C, Healy SD (2014) Measuring variation in cognition. Behav Ecol 25:1287–1292.  https://doi.org/10.1093/beheco/aru090 CrossRefGoogle Scholar
  56. Schmidt KL, McCallum ES, MacDougall-Shackleton EA, MacDougall-Shackleton SA (2013) Early-life stress affects the behavioural and neural response of female song sparrows to conspecific song. Anim Behav 85:825–837.  https://doi.org/10.1016/j.anbehav.2013.01.029 CrossRefGoogle Scholar
  57. Searcy WA, Nowicki S (2019) Birdsong learning, avian cognition, and the evolution of language. Anim Behav. 151:217–227.  https://doi.org/10.1016/j.anbehav.2019.01.015 CrossRefGoogle Scholar
  58. Searcy WA, Nowicki S (2005) The evolution of animal communication: reliability and deception in signaling systems. Princeton University PressGoogle Scholar
  59. Sewall KB, Anderson RC, Soha JA, Peters S, Nowicki S (2018) Early life conditions that impact song learning in male zebra finches also impact neural and behavioral responses to song in females. Dev Neurobiol 10:11.  https://doi.org/10.1002/dneu.22600 CrossRefGoogle Scholar
  60. Shaw RC, Boogert NJ, Clayton NS, Burns KC (2015) Wild psychometrics: evidence for “general” cognitive performance in wild New Zealand robins, Petroica longipes. Anim Behav 109:101–111.  https://doi.org/10.1016/j.anbehav.2015.08.001 CrossRefGoogle Scholar
  61. Shettleworth SJ (2012) Modularity, comparative cognition and human uniqueness. Philos Trans R Soc B 367:2794–2802.  https://doi.org/10.1098/rstb.2012.0211 CrossRefGoogle Scholar
  62. Snowberg LK, Benkman CW (2009) Mate choice based on a key ecological performance trait. J Evol Biol 22:762–769.  https://doi.org/10.1111/j.1420-9101.2009.01699.x CrossRefPubMedGoogle Scholar
  63. Stoffer B, Uetz GW (2015) The effects of social experience with varying male availability on female mate preferences in a wolf spider. Behav Ecol Sociobiol 69:927–937.  https://doi.org/10.1007/s00265-015-1904-2 CrossRefGoogle Scholar
  64. Tchernichovski O, Nottebohm F, Ho CE, Pesaran B, Mitra PP (2000) A procedure for an automated measurement of song similarity. Anim Behav 59:1167–1176.  https://doi.org/10.1006/anbe.1999.1416 CrossRefPubMedGoogle Scholar
  65. ten Cate C (1985) Directed song of male zebra finches as a predictor of subsequent intra- and interspecific social behaviour and pair formation. Behav Processes 10:369–374.  https://doi.org/10.1016/0376-6357(85)90037-3 CrossRefPubMedGoogle Scholar
  66. Tschirren B, Rutstein AN, Postma E, Mariette M, Griffith SC (2009) Short- and long-term consequences of early developmental conditions: a case study on wild and domesticated zebra finches. J Evol Biol 22:387–395.  https://doi.org/10.1111/j.1420-9101.2008.01656.x CrossRefPubMedGoogle Scholar
  67. Tudor MS, Morris MR (2009) Experience plays a role in female preference for symmetry in the swordtail fish xiphophorus malinche. Ethology 115:812–822.  https://doi.org/10.1111/j.1439-0310.2009.01676.x CrossRefGoogle Scholar
  68. Willis PM, Ryan MJ, Rosenthal GG (2011) Encounter rates with conspecific males influence female mate choice in a naturally hybridizing fish. Behav Ecol 22:1234–1240.  https://doi.org/10.1093/beheco/arr119 CrossRefGoogle Scholar
  69. Woodgate JL, Leitner S, Catchpole CK, Berg ML, Bennett ATD, Buchanan KL (2011) Developmental stressors that impair song learning in males do not appear to affect female preferences for song complexity in the zebra finch. Behav Ecol 22:566–573.  https://doi.org/10.1093/beheco/arr006 CrossRefGoogle Scholar
  70. Zann RA (1996) The zebra finch: a synthesis of field and laboratory studies, vol. 5. Oxford University Press, OxfordGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Ecology and Evolutionary BiologyTulane UniversityNew OrleansUSA
  2. 2.Department of Ecology and Evolutionary BiologyUniversity of TennesseeKnoxvilleUSA
  3. 3.Department of Biological SciencesFlorida Atlantic UniversityDavieUSA

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