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Evolution of Bower Complexity and Cerebellum Size in Bowerbirds

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Evolution of Bower Complexity and Cerebellum Size in Bowerbirds Original Paper Brain Behav Evol 2005;66:62–72 Received: September 1, 2004 Returned for revision: September 21, 2004 DOI: 10.1159/000085048 Accepted after revision: January 3, 2005 Published online: April 25, 2005 Evolution of Bower Complexity and Cerebellum Size in Bowerbirds a–c d b Lainy B. Day David A. Westcott Deborah H. Olster a b Departments of Ecology, Evolution, and Marine Biology and Psychology, University of California, c Santa Barbara, Calif. , USA; Department of Zoology and Tropical Ecology, School of Tropical Biology, d James Cook University, Townsville , CSIRO Sustainable Ecosystems and Rainforest CRC, Atherton , Australia Key Words Introduction Birds Bowerbirds Cerebellum Hippocampus Sexual selection Males of the bowerbird family (Ptilonorhynchidae), except three monogamous species, build elaborate dis- play sites (bowers) used to entice females to mate [Mar- Abstract shall, 1954; Kusmierski et al., 1997]. Bower design ap- To entice females to mate, male bowerbirds build elabo- pears to have been sexually selected through female choice rate displays (bowers). Among species, bowers range in as females of several species are known to select mates complexity from simple arenas decorated with leaves to based at least partially on the quality of the bower or the complex twig or grass structures decorated with myriad number of particular items used to decorate the bower colored objects. To investigate the neural underpinnings [Borgia and Mueller, 1992; Madden, 2003a]. Each species of bower building, we examined the contribution of vari- of bowerbird has a particular bower style and preference ation in volume estimates of whole brain (WB), telen- for decorations of certain types or colors [Marshall, 1954; cephalon minus hippocampus (TH), hippocampus (Hp) Madden, 2003b]. Some species build simple or rough- and cerebellum (Cb) to explain differences in complexity hewn bowers, whereas others build intricate, complex, of bowers among 5 species. Using independent con- precisely decorated structures [Marshall, 1954; Kusmier- trasts, we found a signifi cant relationship between bow- ski et al., 1997]. er complexity and Cb size. We did not fi nd support for Previous research has shown that endocranial volume correlated evolution between bower complexity and in bowerbirds is associated with bower complexity, sug- WB, TH, or Hp volume. These results suggest that skills gesting that the diversity of skills associated with bower supported by the cerebellum (e.g., procedural learning, building has led to the evolution of size increases in sev- motor planning) contribute to explaining the variation in eral brain regions concomitantly with increasing bower bower complexity across species. Given that male mat- complexity [Madden, 2001]. This might refl ect the expan- ing success is in part determined by female choice for sion, in concert, of several independent neural regions to bower design, our data are consistent with the hypoth- support a complex suite of behaviors, or may suggest that esis that sexual selection has driven enlargement of the selection for general intelligence and thus larger brains cerebellum in bowerbirds. has allowed for the behavior. In other species, increases Copyright © 2005 S. Karger AG, Basel © 2005 S. Karger AG, Basel Lainy B. Day Department of Physiological Science, University of California Fax +41 61 306 12 34 Los Angeles, CA 90095-1527 (USA) E-Mail [email protected] Accessible online at: Tel. +1 310 825 4170, Fax +1 310 206 9184 www.karger.com www.karger.com/bbe E-Mail [email protected] in whole brain size are associated with behavioral suites regions among bowerbirds and offers a unique opportu- that are thought to demand general intelligence, such as nity to infer which brain regions might be involved in sociality and tool use [Lefebvre et al., 2002; Reader and aspects of bower building. Laland, 2002]. Independent of Madden [2001], we hy- pothesized that brain size might be related to bower com- plexity. Given that changes in whole brain (WB) are often Materials and Methods the result of changes in telencephalon volume we also ex- amined relationships between telencephalon size and Subjects Sixteen male breeding, bower-owning bowerbirds (or giving bower complexity. To go beyond these general measures territorial calls in the case of spotted catbirds) were captured in and in order to begin to explore more specifi c neural un- North Queensland, Australia using mistnets or cagetraps (4 gold- derpinnings of bower building, we also hypothesized that en bowerbirds Prionodura newtonia , 4 toothbill bowerbirds Sceno- the size of particular neural regions, the hippocampus poeetes dentirostris , 4 great bowerbirds Chlamydera nuchalis , 2 satin bowerbirds , and 2 spotted cat- (Hp) and cerebellum (Cb), might be related to bower com- Ptilonorhynchus violaceus birds Ailuroedus crassirostris ). Bower ownership was determined plexity. by long term observations in banded populations or focal obser- If variation in bower design is associated with dif- vations for non-banded populations. Breeding status was judged ferences in the size of particular brain regions, we may by behavior at the bower and confi rmed by testis size and histo- infer that a known function of that brain region could logical condition (bunched spermatozoa). Only one bowerbird of a species was collected from any one geographic region. All spe- be critical for bower building. Brain region/behavior cies used are listed as common in their range [Simpson and Day, relationships have been found in other species. For 1996] and are not listed in any threat category [IUCN, 2003; Cen- instance, in avian species relationships have been tre, 2004]. All protocols were approved by the relevant animal found between hippocampal volume and food storing, care and use committees of the University of California, Santa HVC volume and song complexity, and mesopallium Barbara, James Cook University, Townsville, Queensland and CSIRO Atherton, Queensland and appropriate permits were ac- volume and innovative feeding styles [Sherry et al., quired from Queensland Parks and Wildlife Services. 1992; Brenowitz, 1997; Timmermans et al., 2000; Day 2003]. Bower Traits Our study had two aims: First, we sought to determine The fi ve species studied offered a range of bower types ( fi g. 1 ) if bower building is generally associated with an increase as we personally observed (L.B.D and D.A.W.) and as described in published accounts. Spotted catbirds do not build a bower. Tooth- in volume of WB, Telencephalon minus Hp (TH), Hp or bill bowerbirds clear a patch of ground and decorate this court with Cb by comparing four bower building bowerbirds (fam- upturned leaves [Marshall, 1954]. Golden bowerbirds build a one- ily Ptilonorhynchidae) with a bowerbird that does not or two-tower ‘maypole’ bower that varies greatly in design and size build a bower, the spotted catbird (family Ptilonorhyn- among individuals [Frith and Frith, 2000b]. A display stick is dec- chidae, Ailuroedus crassirostris). Secondly, we tested the orated with lichen and whitish-yellow bracts or fl owers. Satin bow- erbirds build a small avenue bower (approximately 20 cm long by hypothesis that the volumes of WB, TH and neural re- 30 cm wide) with thin sticks and decorate a single court. The court gions known to be involved in spatial or procedural is covered with straw and decorated with mainly yellow and blue skills, hippocampus and cerebellum respectively, are as- natural and manmade objects such as feathers, fl owers, insect ely- sociated with variation in bower design. As the hippo- tra, and plastic objects [Borgia, 1985]. Finally, great bowerbirds campus is known to support avian spatial memory [Sher- build a large avenue bower (approximately 70 cm long by 50 cm wide), decorated with color/location specifi city on the front, the ry et al., 1992], we predicted that hippocampal volume rear, one side and the interior (unpublished observations). These would be greater in species that use larger numbers and decorations are natural or manmade, principally gray, green and types of ornaments and whose nearest neighbor distanc- red objects, such as snail shells, glass, fruits, seeds, and plastic [Mar- es are greatest, as this would demand memory for more shall, 1954]. locations in order to collect ornaments and for memory Scoring Bower Characteristics of greater distances to steal from and destroy neighbors’ We constructed an index to score bowers for general complexity. bowers. The cerebellum is involved in learning proce- We used the guidelines described by Madden [2001], considering dures by observation [Graziano et al., 2002]. We pre- the bowers’ structural complexity (size and number of walls or tow- dicted that cerebellum volume would be related to the ers) and ornamentation (number, diversity). These bower charac- structural complexity and precision of bower design, as teristics were obtained by a combination of personal observations and consensus reports from other authors [Marshall, 1954; Kus- this feature appears to be at least partially learned by mierski et al., 1997; Frith and Frith, 2000a]. In addition, we con- observation and practice [Collis and Borgia, 1993]. Our sidered elements of the display that would be related to the particu- work is the fi rst to compare the size of particular brain lar skills and brain areas of interest. Figure 1 lists bower attributes Evolution of Bower Complexity and Brain Behav Evol 2005;66:62–72 63 Cerebellum Size in Bowerbirds Tree Species General Spatial Procedural Index • Precise
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