Pairs of individuals breed together only if they recognize each other as the same species, but the process of recognizing conspecifics can depend on flexible criteria even when species-specific signals are innate and fixed. This study examines species recognition in naturally hybridizing sister species, California and Gambel’s quail (Callipepla californica and Callipepla gambelii), that have vocalizations which are not learned. Specifically, this study tests whether being raised in a vocalizing mixed-species cohort affects neural activity in the adult auditory forebrain in response to heterospecific and conspecific calls. After hatching, quail chicks were raised either with their own kind or with both species. Once reaching reproductive condition, each adult was played a recording that was one of three types: Gambel’s quail opposite-sex contact calls; California quail opposite-sex contact calls; or synthetic tones. Brains were collected following playback and assessed for neuronal activity by quantifying expression of the protein of the immediate early gene, ZENK, in two brain regions, the caudomedial nidopallium (NCM) and the caudomedial mesopallium (CMM). ZENK levels were greater in NCM of males than females, but female NCM cells responded differentially to conspecific compared to heterospecific calls. Namely, females had more immuno-positive NCM cells when they heard conspecific calls rather than heterospecific male calls. Early experience with heterospecific broodmates did not alter neural responses in the NCM or CMM to heterospecific vocalizations. This study suggests that the NCM plays a role in species discrimination but that rearing condition does not alter the response in these non-vocal-learning species.

Keywords:
Species discrimination, Vocalization, Zenk, Forebrain, Caudomedial nidopallium, Mesopallium, Quail
1.
Adkins-Regan E (2005) Hormones and animal social behavior. Princeton, NJ: Princeton University Press.
2.
Bailey DJ, Wade J (2005) FOS and ZENK responses in 45-day-old zebra finches vary with auditory stimulus and brain region, but not sex. Behav Brain Res 162:108–115.
3.
Bailey DJ, Rosebush JC, Wade J (2002) The hippocampus and caudomedial neostriatum show selective responsiveness to conspecific song in the female zebra finch. J Neurobiol 52:43–51.
4.
Bailey NW, Zuk M (2008) Acoustic experience shapes female mate choice in field crickets. Proc R Soc Lond B 275:2645–2650.
5.
Balaban E (1997) Changes in multiple brain regions underlie species differences in complex, congenital behavior. Proc Natl Acad Sci USA 100:4873–4878.
6.
Ball GF, Balthazart J (2001) Ethological concepts revisited: Immediate early gene induction in response to sexual stimuli in birds. Brain Behav Evol 5:252–270.
7.
Bateman AJ (1948) Intra-sexual selection in Drosophila. Heredity 2:349–368.
8.
Baylé JD, Ramade F, Oliver J (1974) Stereotaxic topography of the brain of the quail (Coturnix coturnix japonica). J Physiol Paris 68:219–241.
9.
Bolhuis JJ, Zijlstra GGO, Den Boer-Visser AM, Van der Zee EA (2000) Localized neuronal activation in the zebra finch brain is related to the strength of song learning. Proc Natl Acad Sci USA 97:2282–2285.
10.
Calkins JD (2007) The family behavior of California Quail: a molecular analysis. Condor 109:962–967.
11.
Calkins JD, Burley NT (2003) Mate choice for multiple ornaments in the California quail, Callipepla californica. Anim Behav 65:69–81.
12.
Ceugniet M, Aubin T (2001) The rally call recognition in males of two hybridizing partridge species, red-legged (Alectoris rufa) and rock (A. graeca) partridges. Behav Proc 55:1–12.
13.
Cornwallis CK, Birkhead TR (2008) Plasticity in reproductive phenotypes reveals status specific correlations between behavioral, morphological and physiological sexual traits. Evolution 62:1149–1161.
14.
Den Hartog PM, de Kort SR, ten Cate C (2007) Hybrid vocalizations are effective within, but not outside, an avian hybrid zone. Behav Ecol 18:608–614.
15.
Deregnaucourt S, Guyomarc’h JC (2003) Mating call discrimination in female European (Coturnix c. coturnix) and Japanese Quail (Coturnix c. japonica). Ethology 109:107–119.
16.
Ellis CR Jr, Stokes AW (1966) Vocalizations and behavior in captive Gambel quail. Condor 68:72–80.
17.
Freeberg TM, Duncan SD, Kast TL, Enstrom DA (1999) Cultural influences on female mate choice: an experimental test in cowbirds, Molothrus ater. Anim Behav 57:421–426.
18.
Gee JM (2003) How a hybrid zone is maintained: behavioral mechanisms of interbreeding between California and Gambel’s quail (Callipepla californica and C. gambelii). Evolution 57:2407–2415.
19.
Gee JM (2005) No species barrier by call in an avian hybrid zone between California and Gambel’s quail (Callipepla californica and C. gambelii) Biol J Linn Soc 86:253–264.
20.
Gentner TG, Margoliash D (2003) Neuronal populations and single cells representing learned auditory objects. Nature 424:669–674.
21.
Good TP, Ellis JC, Annett CA, Pierotti R (2000) Bounded hybrid superiority in an avian hybrid zone: effects of mate, diet and habitat choice. Evolution 54:1774–1783.
22.
Grinnell J, Bryant HC, Storer TI (1918) The Game Birds of California. Berkley, CA: University of California Press.
23.
Hamilton WD (1971) Geometry for the selfish herd. J Theor Biol 31:295–311.
24.
Hebets EA, Wesson J, Shamble PS (2008) Diet influences mate choice selectivity in adult female wolf spiders. Anim Behav 76:355–363.
25.
Hernandez AM, MacDougall-Shackleton SA (2004) Effects of early song experience on song preferences and song control and auditory brain regions in female house finches (Carpodacus mexicanus). J Neurobiol 59:247–258.
26.
Hernandez AM, Phillmore LS, MacDougall-Shackleton SA (2008) Effects of learning on song preferences and Zenk expression in female songbirds. Behav Proc 77:278–284.
27.
Hoke KL, Ryan MJ, Wilczynski W (2008) Candidate neural locus for sex differences in reproductive decisions. Biol Lett 4:518–521.
28.
Hubbs CL (1955) Hybridization between fish species in nature. Syst Zoo 4:1–20.
29.
Jin H, Clayton DF (1997) Localized changes in immediate early gene regulation during sensory and motor learning in zebra finches. Neuron 19:1049–1059.
30.
Lauay C, Gerlach NM, Adkins-Regan E, DeVoogd TJ (2004) Female zebrafinches require early song exposure to prefer high-quality song as adults. Anim Behav 68:1249–1255.
31.
Long KD, Kennedy G, Salbaum JM, Balaban E (2002) Auditory stimulus-induced changes in immediate-early gene expression related to an inborn perceptual predisposition. J Comp Physiol A 188:25–38.
32.
Lorenz K (1935) Der Kumpan in der Umwelt des Vogels. J Ornithol 83:137–413.
33.
Lott DF, Mastrup SNA (1999) Facultative communal brood rearing in California Quail. Condor 101:678–681.
34.
MacDougall-Shackleton SA, MacDougall-Shackleton EA, Hahn TP (2001) Physiological and behavioural responses of female mountain white-crowned sparrows to natal and foreign-dialect songs. Can J Zool 79:325–333.
35.
Maney DL, Cho E, Goode CT (2006) Estrogen-dependent selectivity of genomic responses to birdsong. Eur J Neurosci 23:1523–1529.
36.
Maney DL, Goode CT, Lange HS, Sanford SE, Solomon BL (2008) Estradiol modulates neural responses to song in a seasonal songbird. J Comp Neurol 511:173–186.
37.
Maney DL, MacDougall-Shackleton EA, MacDougall-Shackleton SA, Ball GF, Hahn TP (2003) Immediate early gene response to hearing song correlates with receptive behavior and depends on dialect in a female songbird. J Comp Physiol A 189:667–674.
38.
Marler P, Doupe AJ (2000) Singing in the brain. Proc Natl Acad Sci USA 97:2965–2967.
39.
McLean DD (1930) The Quail of California. Calif. Div. Fish Game. Game Bull. No. 2.
40.
Mello CV, Clayton DF (1994) Song-induced ZENK gene expression in auditory pathways of songbird brain and its relation to the song control system. J Neurosci 14:6652–6666.
41.
Mello CV, Ribeiro S (1998) ZENK protein regulation by song in the brain of songbirds. J Comp Neurol 393:426–438.
42.
Mello CV, Vicario DS, Clayton DF (1992) Song presentation induces gene expression in the songbird forebrain. Proc Natl Acad Sci USA 89:6818–6822.
43.
Pierotti R, Annett CA (1993) Hybridization and male parental care in birds. Condor 95:670–679.
44.
Qvarnström A, Brommer JE, Gustafsson L (2006) Testing the genetics underlying the co-evolution of mate choice and ornament in the wild. Nature 441:84–86.
45.
Riebel K, Smallegange IM, Terpstra NJ, Bolhuis JJ (2002) Sexual equality in zebra finch song preference: evidence for a dissociation between song recognition and production learning. Proc R Soc Lond B Biol Sci 269:729–733.
46.
Sewall KB (2009) Limited adult vocal learning maintains call dialects but permits pair-distinctive calls in red crossbills. Anim Behav 77:1303–1311.
47.
Sewall KB, Hahn TP (2009) Social experience modifies behavioural responsiveness to a preferred vocal signal in red crossbills, Loxia curvirostra. Anim Behav 77:123–128.
48.
Sisneros JA, Forlano PM, Deitcher DL, Bass AH (2004) Steroid-dependent auditory plasticity leads to adaptive coupling of sender and receiver. Science 305:404–407.
49.
Sockman KW (2007) Neural orchestration of mate-choice plasticity in songbirds. J Ornithol 148(suppl 2):S225–S230.
50.
Sockman KW, Gentner TQ, Ball GF (2002) Recent experience modulates forebrain gene expression in response to mate-choice cues in European starlings. Proc R Soc Lond B 269:2479–2485.
51.
Sockman KW, Gentner TQ, Ball GF (2005) Complementary neural systems for the experience-dependent integration of mate-choice cues in European starlings. J Neurobiol 62:72–81.
52.
Stripling R, Kruse AA, Clayton DF (2001) Development of song responses in the zebra finch caudomedial neostriatum: role of genomic and electrophysiological activities. J Neurobiol 48:163–180.
53.
Ten Cate C, Vos DR, Mann N (1993) Sexual imprinting and song learning; two of one kind? Neth J Zool 43:34–45.
54.
Terpstra NJ, Bolhuis JJ, den Boer-Visser AM, ten Cate C (2005) Neuronal activation related to auditory perception in the brain of non-songbird, the Ring Dove. J Comp Neurol 488:342–351.
55.
Terpstra NJ, Bolhuis JJ, Riebel K, van der Burg JM, den Boer-Visser AM (2006) Localized brain activation specific to auditory memory in a female songbird. J Comp Neurol 494:784–791.
56.
Tomaszycki ML, Sluzas EM, Sundberg KA, Newman SW, DeVoogd TJ (2006) Immediate early gene responses to song in juvenile female and male Zebra Finches: Effects of rearing environment. J Neurobiol 66:1175–1182.
57.
Uetz GW, Norton S (2007) Preference for male traits in female wolf spiders varies with the choice of available males, female age and reproductive state. Behav Ecol Sociobiol 61:631–641.
58.
Williams HW (1969) Vocal behavior of adult California Quail. Auk 86:631–659.
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