Cognition and the Brain of Brood Parasitic Cowbirds

Western University Scholarship@Western

Psychology Publications Psychology Department

3-1-2019

Cognition and the brain of brood parasitic cowbirds.

David F Sherry

Mélanie F Guigueno

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Citation of this paper: Sherry, David F and Guigueno, Mélanie F, "Cognition and the brain of brood parasitic cowbirds." (2019). Psychology Publications. 175. https://ir.lib.uwo.ca/psychologypub/175 Integrative Zoology 2019; 14: 145–157 doi: 10.1111/1749-4877.12312

1 REVIEW 1 2 2 3 3 4 4 5 5 6 6 7 Cognition and the brain of brood parasitic cowbirds 7 8 8 9 9 10 10 11 David F. SHERRY1 and Mélanie F. GUIGUENO2 11 12 12 1 2 13 Department of Psychology, Western University London, Ontario and Department of Natural Resource Sciences, McGill University, 13 14 Montreal, Quebec, Canada 14 15 15 16 16 17 17 18 18 19 Abstract 19 20 Cowbirds are brood parasites. Females lay their eggs in the nests of other species, which then incubate the cow- 20 21 bird eggs and raise the young cowbirds. Finding and returning to heterospecific nests presents cowbirds with 21 22 several cognitive challenges. In some species, such as brown-headed cowbirds (Molothrus ater), females but 22 23 not males search for and remember the locations of potential host nests. We describe recent research on sex dif- 23 24 ferences in cognition and the hippocampus associated with this sex difference in search for host nests. Female 24 25 brown-headed cowbirds perform better than males on some, but not all, tests of spatial memory and females 25 26 show a pattern of adult hippocampal neurogenesis not found in males or in closely related non-parasitic birds. 26 27 Because of the apparent specialization of the hippocampus, brown-headed cowbirds may be a good model in 27 28 which to examine spatial information processing in the avian hippocampus and we also describe recent research 28 29 on the spatial response properties of brown-headed cowbird hippocampal neurons. 29 30 30 31 Key words: adult neurogenesis, brood parasites, cowbirds, hippocampus, sex differences, spatial memory 31 32 32 33 33 34 34 35 35 this brood parasitic way of life. Selection should be no 36 INTRODUCTION 36 less intense on brood parasites than on non-parasites, 37 37 Brood parasites avoid the costs of nest building, incu- and non-parasites possess a vast range of behavioral, 38 38 bation and parental care by laying their eggs in the nests cognitive, physiological and neural specializations that 39 39 of other birds. For obligate brood parasites, there is no promote successful reproduction (Lack 1972; Williams 40 40 other path to successful reproduction. It therefore seems 2012; Deeming & Reynolds 2016). The present paper 41 41 reasonable to suppose that natural selection has acted describes cognition and the brain of brood parasites, fo- 42 42 on behavior, cognition and the brain of brood parasites cusing on recent research on sex differences in spatial 43 43 to increase individual reproductive success achieved by memory and the hippocampus of cowbirds. 44 44 45 There are 6 major groups of interspecific brood par- 45 46 asites: cowbirds, honeyguides, parasitic finches, Old 46 47 World cuckoos, New World ground-cuckoos, and 1 spe- 47 48 Correspondence: David Sherry, Advanced Facility for Avian cies of parasitic duck (Davies 2000). To succeed in hav- 48 49 Research, Department of Psychology, Western University, ing heterospecific parents incubate their eggs and raise 49 50 London ON N6G 1G9, Canada. their young, brood parasites have to solve a number of 50 51 Email: [email protected] problems that non-parasites do not, and many of these 51

1 problems are cognitive: brown-headed cowbirds (Jetz et al. 2008). Brown-head- 1 2 1. Find potential host nests. Most songbird hosts of ed cowbirds probably do not achieve a 10-fold repro- 2 3 cowbirds take a great deal of care to conceal their nests ductive advantage compared to non-parasites from the 3 4 to reduce predation on eggs, nestlings and incubating large number of eggs they produce (Woolfenden et al. 4 5 adults, and to reduce brood parasitism. 2003), but their brood parasitic behavior does require 5 6 2. Remember and revisit potential host nests. Hav- finding and returning to a very large number of potential 6 host nests. 7 ing found a nest, female cowbirds return to it later, ei- 7 8 ther to monitor host clutch completion, to lay one of her Female brown-headed cowbirds search for host nests 8 9 own eggs, or to remove a host egg (Sealy 1992; Scar- in which to lay their eggs but males do not. This di- 9 10 damaglia et al. 2017). vision of labor between the sexes does not occur in 10 all cowbirds. In the South American screaming cow- 11 3. Determine the stage of host clutch completion. Fe- 11 bird (Molothrus rufoaxillaris Cassin, 1866) males and 12 male cowbirds prefer to lay in host nests in which a few 12 females search for host nests together. However, in 13 eggs have been laid but the clutch is not yet complete 13 brown-headed cowbirds, search is performed by fe- 14 to ensure that her egg hatches with or before the host’s 14 15 males alone and it occurs some time before females ac- 15 eggs (Sealy 1995). tually lay their parasitic egg. Females often lay at dawn, 16 4. Monitor the host’s response to brood parasitism 16 17 or earlier (Neudorf & Sealy 1994), and so they are not 17 (Hoover & Robinson 2007) and the reproductive out- searching at this time for potential host nests. They are 18 18 come of the cowbird’s brood parasitic behavior (Louder going to a nest they have previously discovered. After 19 19 et al. 2015). laying, they may spend the rest of the morning search- 20 20 Some of the cognitive processes involved in brood ing for host nests in which to lay eggs on subsequent 21 21 parasitism have been examined in current research. days (Scott 1991), or re-visiting nests they have already 22 22 These include spatial memory, especially sex differenc- discovered to check on the progress of host egg laying 23 23 es in spatial memory (Astié et al. 1998; Guigueno et al. and clutch completion (White et al. 2009). Females find 24 2014, 2015; Astié et al. 2015), numerical ability (White nests by flying into understory vegetation to flush in- 24 25 et al. 2007, 2009) and specializations in the brain that cubating hosts or by watching the nest building behav- 25 26 accompany these cognitive specializations (Sherry et ior of hosts from the canopy or the forest floor (Nor- 26 27 al. 1993; Reboreda et al. 1996; Clayton et al. 1997; man & Robertson 1975). Females are choosy about the 27 28 Nair-Roberts et al. 2006; Guigueno et al. 2016). state of the nest in which they lay their egg. They prefer 28 29 29 The research we describe examines how the brood to lay in a nest that already has some eggs in it, but not 30 30 parasitic mode of reproduction has modified cogni- too many. In fact, female brown-headed cowbirds pre- 31 fer to lay in a host nest with 3 eggs in it, but it is equally 31 tion and the brain of brood parasites. We describe sex important that it be an active nest to which the host par- 32 differences in spatial memory that have been found 32 ent is still adding eggs. David White and his colleagues 33 in brown-headed cowbirds and sex differences in the 33 found that day-to-day changes in the number of eggs in 34 brain, specifically in the size of the hippocampus and 34 a host nest can have a major effect on how likely a fe- 35 in adult hippocampal neurogenesis, that are associat- 35 male brown-headed cowbird is to place one of her own 36 ed with these sex differences in spatial memory. Given 36 eggs in that nest (White et al. 2009). This preference 37 the apparent specialization of the brown-headed cow- 37 for nests with a daily change in egg number occurs be- 38 bird hippocampus, we also describe recent research ex- 38 39 cause a nest in which the number of eggs is unchanging 39 amining the spatial response properties of neurons in the is a nest in which the host has ceased laying and begun 40 40 brown-headed cowbird hippocampus. incubation. If incubation has already begun, there is re- 41 41 ally no way to determine when those eggs are likely to 42 42 SEX DIFFERENCES IN SPATIAL hatch. If they hatch before the cowbird egg has complet- 43 ed development, the cowbird egg will be abandoned and 43 44 MEMORY never hatch. In contrast, a nest to which the host is still 44 45 45 Female brown-headed cowbirds [Molothrus ater adding eggs is a nest in which incubation has not yet be- 46 46 (Boddaert, 1783)], parasitize over 200 different spe- gun, and a cowbird egg placed in such a nest will hatch 47 47 cies of host and can lay up to 40 eggs in a breeding sea- along with or even before the host’s young. 48 48 son (Scott & Ankney 1980, 1983; Rothstein et al. 1987), White et al. (2009) showed that females attend to the 49 49 compared to mean clutch sizes of 4–5 eggs for temper- number of eggs in a host nest by allowing females to in- 50 50 ate zone birds occupying the same geographic range as spect artificial host nests in which the researchers ex- 51 51

1 perimentally manipulated the number of eggs. In one resembled search for host nests, but of course male 1 2 experiment, brown-headed cowbirds were allowed to brown-headed cowbirds do not search for host nests. We 2 3 observe one nest in which the number of eggs was stable therefore used a food rewarded task, but tried to simu- 3 4 at 3 over successive days. In another nest, brown-head- late important elements of spatial search for host nests 4 5 ed cowbirds saw the number of eggs increase from 1 to (Guigueno et al. 2014). Males and females searched an 5 6 2 and from 2 to 3 over successive days. When given the array of covered food cups in a 1.8 × 1.8-m wire mesh 6 7 opportunity to lay their own eggs, female brown-headed enclosure. There were 25 cups arranged in a 5 × 5 pat- 7 8 cowbirds preferred to lay in the nest in which the num- tern and any of the 8 interior cups in the array (the cen- 8 9 ber of eggs increased over successive days. Both nests ter-most cup was excluded) could be baited with food 9 10 contained 3 eggs on test days, but brown-headed cow- (Fig. 1). Birds searched until they found the one baited 10 11 birds had seen the number of eggs change over days in cup, ate the food it contained and then returned to their 11 12 one nest but not the other. To do this in the wild, a fe- home cage. After a delay of 24 h they returned to search 12 male brown-headed cowbird would have to remember 13 the array. The same food cup was baited and birds 13 the spatial location of the nest and reliably return to it 14 searched again. To minimize possible use of olfacto- 14 on successive days. 15 ry cues, all cups were shaken for 15 s with food in them 15 16 Because it is females that search for and revisit po- before each trial. On the following day, a new trial com- 16 tential host nests, it is possible that female cowbirds 17 menced in which a new randomly selected cup was bait- 17 have better spatial memory than males. Sex differences 18 ed, birds searched until they found it, and then had to 18 in spatial memory occur in other animals, usually favor- 19 remember that new spatial location for 24 h. These con- 19 ing males in species in which males have larger home ditions were intended to simulate search for host nests 20 ranges than females (Gaulin 1992). We tested for a sex 20 in which females locate potential host nests and then re- 21 difference in spatial memory in brown-headed cowbirds 21 turn to them the following day, either to monitor host 22 in two ways. In one experiment, brown-headed cow- 22 clutch completion or to lay an egg in the host nest. We 23 bird males and females searched for food hidden in cov- 23 24 ered cups in an indoor enclosure. In another experiment, tested birds in both breeding and non-breeding condi- 24 25 birds performed spatial tests on a touchscreen for food tion, induced in the lab by manipulation of photoperi- 25 26 reward. od and verified by hormone assay, frequency of song by 26 27 males, and egg laying by females. 27 28 SPATIAL SEARCH Females performed better than males at this task, 28 29 making fewer errors before relocating the baited food 29 30 We wished to compare spatial memory between cup on tests and taking more direct paths to the correct 30 31 male and female brown-headed cowbirds in tasks that food cup (Figs 1 and 2). Although our manipulation of 31 32 photoperiod successfully brought birds into breeding 32 33 33 34 34

35 4 35 36 FemalesFemales n = 7 Tortuosity of path to ﬁrst correct choice 36 37 Males 37 3 Males n = 7 38 Females n = 7 38 * * 10 Males n = 7 39 Females 39 2 9 40 Males 40 8 * * 41 Number of Errors 7 41 1 6 42 5 42 43 4 43

0 Path tortuosity

Path tortuosity 3 44 Non-breeding Breeding 44 2 45 Non-‐breeding Breeding 1 45 46 0 46 Figure 1 Female brown-headed cowbirds make fewer errors Non-breeding Breeding 47 than males in a task that requires remembering for 24 h which Non-‐breeding Breeding 47 48 of 8 food cups contained food. There is no effect of breeding Figure 2 Females take more direct paths to a remembered food 48 49 condition. Insert in upper left shows the apparatus. Circles rep- cup than males. There is no effect of breeding condition. Path 49 50 resent food cups, of which any of the 8 shown in gray could be tortuosity equals the ratio of the length of the path taken by the 50 51 randomly baited on a trial. bird (green) to length of the most direct path (red). 51

1 condition as shown by higher androgen levels in males ulus that matched the sample in spatial location on the 1 2 and females, increased song in males and egg laying by screen produced food reward. In another version of the 2 3 some females (Guigueno et al. 2014), there was no ef- task, pecking the stimulus that matched the sample in 3 4 fect of breeding condition on performance of the spatial color produced food reward. The delay between pecking 4 5 memory task. the sample and presentation of the test stimuli was var- 5 6 Females therefore appear to have better spatial mem- ied to produce retention intervals (RIs) of 15, 30, 45 and 6 7 ory than males in a task that resembles, in some ways, 60 s. Males and females were tested in both breeding 7 8 search for potential host nests. This sex difference in and non-breeding condition induced by manipulation of 8 9 spatial ability is the reverse of the sex difference some- photoperiod. 9 10 times found in mammals, in which males exhibit great- Both males and females performed better on the spa- 10 11 er spatial ability than females. The explanation for su- tial version of this task than on the color version (Fig. 4). 11 12 perior male spatial ability that is often given is that There were interesting differences, however, between 12 13 males, depending on breeding system, range more wide- performance on this touchscreen task and performance 13 14 ly in search of mating opportunities than females do on the open field task described previously. On the spa- 14 15 (Gaulin 1992; Sherry et al. 1992). In polygynous mead- tial version of the touchscreen task, males performed 15 16 ow voles [Microtus pennsylvanicus (Ord, 1815)], males better in breeding condition than in non-breeding condi- 16 17 have a larger home range than females, better spatial tion, and males in breeding condition performed better 17 18 ability in laboratory tests and a relatively larger hippo- than females in breeding condition (Fig. 5a). Retention 18 19 campus (Gaulin & FitzGerald 1986, 1989; Jacobs et al. intervals affected male and female performance differ- 19 20 1990). These sex differences are not found in monoga- ently. Males performed better than females at the 15-s 20 21 mous pine [Microtus pinetorum (Le Conte, 1830)] and RI and their performance declined with increasing RI. 21 22 prairie voles [Microtus ochrogaster (Wagner, 1842)] in Female performance was not affected by RI, and there 22 23 which male and female home range size does not differ. was no interaction between RI and breeding condition. 23 24 Among male meadow voles, spatial ability is correlat- 24 25 ed with male home range size and, hence, with the num- 25 26 ber of female meadow voles visited and the number of 26

27 1"27 litters sired (Spritzer et al. 2005). What our results with " 28 brown-headed cowbirds show is that sex differences in 28

29 " 29 spatial ability do not depend strictly on sex but instead " 30 30 on sex-specific patterns in the use of space. In mammals " 31 " 31 in which males compete for mating opportunities by in- 32 " 32 creasing their home range size, natural selection can fa- "

33 " 33 vor better spatial ability in males than in females. In a " " " 34 " 34 species like brown-headed cowbirds, in which females R " 35 35 compete for breeding opportunities by searching for " " 36 36 host nests, natural selection can favor better spatial abil- 37 " 37 ity in females. "

38 " 38 " 39 RI " 39 SPATIAL SEARCH ON A TOUCHSCREEN " 40 40 41 Does the sex difference in spatial ability that we RI = 15, 30, 45, 60 s 41 " 42 " 42 found in brown-headed cowbirds depend on the kind Figure 3 Schematic diagram of space (upper) and color (low- 43 43 of spatial task the birds perform? We designed a sec- er) touchscreen stimuli. Birds first pecked a fixation point (green 44 44 ond task that tested spatial ability but did not resem- circle for the spatial task, white circle for the color task) to 45 ble search for host nests by female brown-headed cow- make a sample stimulus appear on the screen. Pecking the sam- 45 46 birds (Guigueno et al. 2015). In this delayed matching ple stimulus led to retention interval (RI) of 15, 30, 45 or 60 s. 46 47 to sample task, birds pecked a sample stimulus on a Birds then pecked a second fixation point (blue circle for the 47 48 touchscreen and then after a delay pecked the stimulus, spatial task, black circle for the color task) to make the sample 48 49 from among a set of 3 stimuli, that matched the sam- and distractor stimuli appear on the screen. Pecking the correct 49 50 ple (Fig. 3). In one version of the task, pecking the stim- sample among the distractors produced a food reward; pecking 50 51 a distractor produced a 5-s lights out period. 51

1 The only notable effect in the color version of the touch- non-breeding males. Male performance also grew poor- 1 2 screen task (apart from the fact that birds showed lower er with increasing RI whereas female performance did 2 3 accuracy than on the spatial task) was that females per- not. 3 4 formed better in breeding than in non-breeding condi- It is possible there are trade-offs between kinds of 4 5 tion (Fig. 5b). spatial ability (Sherry & Schacter 1987). For females, 5 6 The results of this touchscreen experiment and the dedicating cognitive and neural resources to navigation 6 7 spatial search task described earlier show that sex dif- and memory for real world nest-like spatial locations 7 8 ferences in spatial ability depend on the way in which may come at the cost of performance on other tasks that 8 9 spatial ability is tested. Indeed, “spatial ability” like- 9 10 ly consists of multiple abilities that differ in the kind of 10 11 stimuli that are processed and the behaviors they influ- 11 12 ence. The open field task (Guigueno et al. 2014) more 12 13 13 closely resembles search for potential host nests than the a Non-‐breeding 14 touchscreen task (Guigueno et al. 2015). It required an- 14 15 15 imals to search for one location among many, and, hav- 0.8 Breeding * 16 ing found it, to remember that location for 24 h. In the 16 17 17 following trial, birds had to search for a new baited lo- 0.75 18 cation that would be rewarded 24 h later. The task re- * 18 19 19 quired locomotion and navigation in a 1.8 × 1.8-m space 0.7 20 and females performed better on this task than males 20 21 in both the directness of their path to the correct loca- 0.65 21 22 tion and the number of errors they made before getting 22 23 23

there. On the touchscreen task, birds were shown a stim- Proportion correct 0.6 24 ulus on a vertical surface a few centimeters in front of 24 25 them, had to remember this stimulus for up to 60 s, and 0.55 25 26 then identify it again embedded among distractor stimu- 26 27 li. No locomotion or navigation were involved. Instead, 0.5 27 28 birds had to remember a location (or a color) presented Males Males Females Females 28 29 in their near visual field. Breeding males performed best 29 30 30 at this task, better than breeding females and better than b Non-‐breeding 31 Non-breeding 31 32 32 0.58 Breeding Breeding 33 33 34 0.53 34 35 Spa&al 35 Colour * 36 0.48 36 37 0.8 37 Spatial Proportion correct 38 0.7 0.43 38 Color 39 39 0.6 * * 40 0.38 40 0.5 41 41 0.4 0.33 42 -‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐-‐ 42 Proportion correct Males Females 43 0.3 Males Females 43 44 0.2 44 Figure 5 (a) Male brown-headed cowbirds in breeding con- 0.1 45 dition performed better than females in breeding condition 45 46 0 46 Females Males and better than males in non-breeding condition on the spatial 47 Females Males touchscreen task. (b) Female brown-headed cowbirds in breed- 47 48 Figure 4 Female and male brown-headed cowbirds both per- ing condition performed better than females in non-breeding 48 49 formed better on the spatial than the color touchscreen task. All condition in the color task. There was no overall significant dif- 49 50 birds performed above chance (horizontal line) on both tasks. ference between the sexes on the color task. Asterisks indicate 50 51 Asterisks indicate a significant difference, P < 0.05 a significant difference,P < 0.05. 51

1 have a spatial component. It is also possible, howev- ferences in cognition between individuals are the out- 1 2 er, that superior male performance on the spatial touch- come of neural differences and sex differences in spa- 2 3 screen task reflects specialization for some unknown be- tial cognition are likely to involve the hippocampus. 3 4 havior that requires relatively short-lasting memory for The first investigation of possible sex differences in the 4 5 proximal spatial location, and the improvement in per- hippocampus of cowbirds compared the size of the hip- 5 6 formance on the spatial touchscreen task that comes pocampus, relative to the size of the telencephalon (or 6 7 with breeding condition in males but not females sug- forebrain), in male and female brown-headed cowbirds 7 8 gests that this may be the case. and a closely-related non-parasite, the red-winged black- 8 9 The improvement that occurs in performance of birds [(Agelaius phoeniceus (Linnaeus, 1766); Sherry et 9 10 the touchscreen color task that occurs in females only al. 1993]. The results showed that female brown-headed 10 11 during breeding condition could, similarly, reflect spe- cowbirds had a larger hippocampus, relative to the size 11 12 cialization for a behavior they perform in the wild. Male of their telencephalon, than male brown-headed cow- 12 13 brown-headed cowbirds have an iridescent black plum- birds and that no sex difference occurred in red-winged 13 14 age that contrasts with their chocolate brown head, and blackbirds. In addition, brown-headed cowbirds had a 14 15 females may use and remember iridescent color in or- larger hippocampus than red-winged blackbirds, de- 15 16 der to choose among potential mates in a way that males spite having a smaller telencephalon than the larger red- 16 17 do not. The plumage of nutritionally stressed male winged blackbirds (mean weights: red-winged black- 17 18 brown-headed cowbirds has a different hue and low- birds 47.7 g; brown-headed cowbird 39.7 g). 18 19 er brightness and saturation than the plumage of males The most likely explanation for this sex difference 19 20 fed ad libitum (McGraw et al. 2002). It is also possible in relative hippocampal size is that selection for spa- 20 21 that female brown-headed cowbirds discriminate among tial ability, and in particular memory for the spatial lo- 21 22 hosts based on host egg color, which could lead to im- cations of potential host nests, has acted differentially 22 23 proved short-term memory for color stimuli in females on female compared to male brown-headed cowbirds. 23 24 but not males during breeding. In the absence of such sex-specific selection, no sex 24 25 25 These hypotheses, however, require testing. Fur- difference in hippocampal size occurs in red-winged 26 26 ther tests of the idea that superior female spatial abili- blackbirds. Brood parasitism is not the only difference 27 27 ty is associated with search for host nests could be per- between brown-headed cowbirds and red-winged black- 28 28 formed in large enclosures (e.g. White et al. 2017) that birds; they differ in territoriality, mating system, male 29 29 more closely resemble the spatial scale at which females aggression, song learning and social development, al- 30 30 search for host nests. Superior performance by male though both are medium range migrants, have similar 31 31 brown-headed cowbirds in breeding condition on the diets and feed away from the areas of reproductive ac- 32 32 touchscreen spatial task is puzzling but the domain of tivity, which are forests, forest edges and woodlands for 33 33 this sex difference could be further examined by vary- brown-headed cowbirds and small nesting territories 34 34 ing the kind of spatial task presented on the touchscreen, within colonies for red-winged blackbirds. However, 35 35 in more naturalistic foraging tasks or in tests of memo- specific ecological selection pressures resulting in a sex 36 36 ry for the spatial location of females. Similarly, the do- difference in hippocampal size are likely to involve spa- 37 37 main of superior performance by breeding females on tial behavior (Sherry et al. 1992). 38 38 the touchscreen color task could be examined in tests of Subsequent research with South American cowbirds 39 39 discrimination by females between potential mates or in has supported this conclusion. Reboreda et al. (1996) 40 40 tests using host eggs as stimuli. examined the hippocampus of 3 species of cowbirds, the 41 41 shiny cowbird [Molothrus bonariensis (Gmelin, 1789)], 42 42 a generalist brood parasite like the brown-headed cow- 43 SEX DIFFERENCES IN THE BRAIN 43 bird, the screaming cowbird (Molothrus rufoaxillar- 44 44 is), a specialist brood parasite that parasitizes primar- 45 Hippocampal size 45 ily the grayish baywing [Agelaioides badius (Vieillot, 46 46 Sex differences in cognition are the outcome of sex 1819) formerly known as the bay-winged cowbird Mo- 47 47 differences in the brain. Whether sex differences in cog- lothrus badius (Vieillot, 1819)], and the non-parasit- 48 48 nition are the result of sexual development and differ- ic grayish baywing. Shiny cowbird females search for 49 49 entiation or the outcome of differences in individual host nests unassisted by males, and like brown-head- 50 50 experience, whether they are inflexible or transient, dif- ed cowbirds, parasitize several hundred species of host. 51 51

1 Screaming cowbird females and males search togeth- changes in size seasonally in a rough correlation with 1 2 er for nests of the grayish baywing. Grayish baywings the waxing and waning of food storing behavior (Sherry 2 3 are not brood parasites and incubate their own eggs and & MacDougall-Shackleton 2015). Clayton et al. (1997) 3 4 raise their own young (and when parasitized, the young examined seasonal change in the hippocampus of the 4 5 of screaming cowbirds). The results showed that both South American cowbirds described above and found 5 6 brood parasites had a larger hippocampus, relative to the that the hippocampus was larger, relative to the size of 6 7 size of the telencephalon, than the non-parasitic gray- the telencephalon, in the breeding season than in the 7 8 ish baywing. Female shiny cowbirds had a larger hip- non-breeding season in both the generalist shiny cow- 8 9 pocampus, relative to the size of the telencephalon, than bird and the specialist screaming cowbird (Clayton et al. 9 10 males but there was no sex difference in relative hippo- 1997). In the shiny cowbird but not the screaming cow- 10 11 campal size in either screaming cowbirds or the gray- bird there was a sex difference in relative hippocampal 11 12 ish baywing. As in the case of brown-headed cowbirds, size in favor of females and there was no interaction be- 12 13 search for host nests by females appears to have selected tween sex and breeding season in relative hippocampal 13 14 for greater hippocampal size in females than in males. size in shiny cowbirds (Clayton et al. 1997) 14 15 When no sex difference in spatial behavior occurs, as in More recent research with brown-headed cowbirds 15 16 red-winged blackbirds, screaming cowbirds and grayish adds further detail to this general picture of seasonal 16 17 baywings, there is also no sex difference in hippocam- change and sex differences in the hippocampus of brood 17 18 pal size. It is notable that even though shiny cowbird fe- parasites. In a study of brown-headed cowbirds and 18 19 males search for host nests and males do not, mean rela- red-winged blackbirds collected during breeding and 19 20 tive hippocampal size is larger in shiny cowbirds than in post-breeding, Guigueno et al. (2016) found that cow- 20 21 screaming cowbirds and grayish baywings, suggesting birds had a larger hippocampus relative to the telenceph- 21 22 that selection acting primarily on females has also acted alon than red-winged blackbirds, females had a great- 22 23 to increase hippocampal size in males, compared to the er relative hippocampal size than males in both species, 23 24 other species examined in this study. Selection on one and there was no effect of breeding season on rela- 24 25 sex can produce phenotypic effects on both sexes be- tive hippocampal size. These findings differ from previ- 25 26 cause most genes are shared by males and females and, ous results showing a sex difference in relative hippo- 26 27 therefore, additional relatively intense sex-specific se- campal size in generalist but not specialist parasites or 27 28 lection is necessary to produce the kind of sex differenc- non-parasites (Sherry et al. 1993; Reboreda et al. 1996), 28 29 es observed in hippocampal size in the generalist brood although one previous study found no sex differences 29 30 parasites (Lande 1980; Wyman et al. 2013). in hippocampal size in any of shiny cowbirds, scream- 30 31 These two examinations of sex differences in the hip- ing cowbirds or grayish baywings (Nair-Roberts et al. 31 32 pocampus (Reboreda et al. 1996; Sherry et al. 1993) 2006). Guigueno et al. (2016) also found no indication 32 33 looked at birds collected during the breeding season: of seasonal change in the size of the hippocampus in ei- 33 34 April to May for brown-headed cowbirds collected in ther brown-headed cowbirds or red-winged blackbirds, 34 35 the northern hemisphere in Canada; and December to in contrast to previous findings with the shiny cowbird 35 36 March for cowbirds collected in the southern hemi- generalist parasite (Clayton et al., 1997). It is not clear 36 37 sphere in Argentina. If greater hippocampal size in fe- why the results of Guigueno et al. (2016) differ from 37 38 males than in males is an adaptation to spatial search previous findings. Specifically, Guigueno et al. (2016) 38 39 and spatial memory involved in finding and remember- found that while a sex difference in favor of females in 39 40 ing potential host nests, then it is possible that it occurs relative hippocampal size, indeed, occurs in a general- 40 41 only during breeding and not at other times of year. Sex ist brood parasite, it also occurs in a non-parasite, and 41 42 differences in the hippocampus of rodents show sea- that there appears to be no seasonal change in relative 42 43 sonal variation correlated with breeding activity (Ga- hippocampal size in brown-headed cowbirds. The sam- 43 44 lea & McEwen 1999; Omerod & Galea 2003; Galea et ple sizes in this study are larger than in previous studies, 44 45 al. 2013). This seasonal variation probably occurs be- plumage and skull pneumatization were used to confirm 45 46 cause brain tissue is expensive. In songbirds, the song that all birds were adults, and breeding condition was 46 47 control nuclei increase in size during breeding when confirmed by androgen assay. The notable result of this 47 48 males are singing to defend territories and attract mates. study was not that there is no sex difference in hippo- 48 49 In food-storing birds like the black-capped chickadee campal size in the brood parasite (there was) but that a 49 50 [Poecile atricapillus (Linnaeus, 1766)] the hippocampus similar sex difference, also in favor of females, occurred 50 51 51

1 in non-parasitic red-winged blackbirds. lar production of new hippocampal neurons than males 1 2 and this sex difference is absent in the non-parasitic red- 2 Hippocampal neurogenesis 3 winged blackbird. In addition, there is more produc- 3 4 We quantified hippocampal neurogenesis in tion of new neurons in the subventricular zone and mi- 4 5 brown-headed cowbirds and red-winged blackbirds us- gration of more new neurons into the hippocampus in 5 6 ing doublecortin (DCX) as a marker for migrating and brown-headed cowbirds following breeding than during 6 7 differentiating neurons. Female brown-headed cow- breeding. In red-winged blackbirds, more new neurons 7 8 birds exhibited greater hippocampal DCX immunore- are found in the hippocampus during breeding than fol- 8 9 activity than males in the neuroproliferative subventric- lowing breeding. One hypothesis to explain this season- 9 10 ular zone, and this sex difference did not occur in red- al effect in brown-headed cowbirds is that the recruit- 10 11 winged blackbirds (Figs 6 and 7; Guigueno et al. 2016). ment of new neurons into the hippocampus following 11 12 In addition, there was a higher level of subventricu- breeding prepares the hippocampus for the subsequent 12 13 lar zone neurogenesis in brown-headed cowbirds in the breeding season and subsequent search for new poten- 13 14 post-breeding period and a difference in the opposite di- tial host nests, either by replacing hippocampal neu- 14 15 rection between the breeding and non-breeding periods rons that have been lost, or acting selectively on mem- 15 16 in red-winged blackbirds. These sex and seasonal dif- 16 17 ferences in hippocampal neurogenesis in brown-head- 17 18 ed cowbirds may be the outcome of specialization of 18 19 the hippocampus of female brown-headed cowbirds 19 20 for locating and remembering potential host nests. Fe- a 20 21 male brown-headed cowbirds show greater subventricu- 21 22 22 23 23 24 24 25 25 26 26 27 27 28 28 29 Cowbirds Blackbirds 29 30 30 31 31 32 b 32 33 33 34 34 35 35 36 36 37 37 38 38 39 39 40 40 Transformed DCX labeling in HP 41 41 42 Cowbirds Blackbirds 42 43 43 Figure 7 (a) Female brown-headed cowbirds show greater 44 44 hippocampal neurogenesis, indicated by doublecortin (DCX) 45 immunoreactivity, than males. No sex difference in hippo- 45 46 campal neurogenesis occurs in red-winged blackbirds. (b) 46 47 Figure 6 (a) The hippocampus of the brown-headed cowbird Brown-headed cowbirds show greater hippocampal neurogene- 47 48 labeled with NeuN to show mature neurons. (b) New hippo- sis post-breeding than during breeding while red-winged black- 48 49 campal neurons labeled with doublecortin, showing a differ- birds show a difference in the opposite direction. SVZ subven- 49 50 entiating neuron (upper black arrow) and a migrating neuron tricular zone, HP hippocampus. Asterisks indicate a significant 50 51 (lower black arrow). difference, P < 0.05. 51

1 ory. There have been many theoretical proposals and a and pattern cells that resemble grid cells in some ways 1 2 great deal of experimental work, most of it in labora- (Kahn et al. 2008). If the hippocampus of brown-head- 2 3 tory rats and mice, on the function of adult hippocam- ed cowbirds, especially female brown-headed cowbirds, 3 4 pal neurogenesis (Gould et al. 1999; Lindsey & Tro- is specialized to process spatial information then we 4 5 pepe 2006; Bruel-Jungerman et al. 2007; Kempermann would expect, at a minimum, that there are cells in the 5 6 2008; van Praag 2008; Aimone et al. 2014; Oomen et brown-headed cowbird hippocampus that are sensitive 6 7 al. 2014; Cameron & Glover 2015). One particularly in- to spatial context. 7 8 teresting idea in the context of cowbird search for host We tested the sensitivity of brown-headed cowbird 8 9 nests is that hippocampal neurogenesis causes forget- hippocampal neurons to spatial context by allowing 9 10 ting by disrupting hippocampal circuitry (Frankland et birds to explore two distinctive spatial environments and 10 11 al. 2013). Forgetting has many benefits, from discard- then visualizing hippocampal neuron activation using 11 12 ing outdated information to reducing proactive interfer- the immediate early gene Egr1 (also known as ZENK, 12 13 ence in memory. Recruitment of new, unbiased neurons Zif268, NGFI-A and Krox-24; Grella et al. 2016). Birds 13 14 into the hippocampus may aid in pattern separation; were trained to find food in 1 of 5 covered bowls in 14 15 that is, distinguishing between new memories that share each of 2 readily discriminable rooms. The rooms dif- 15 16 many properties but also have distinguishing features fered in the colors of the floor and door; one room had a 16 17 (Frankland et al. 2013). Hippocampal neurogenesis fol- distinctive depression in the floor that ran from wall to 17 18 lowing breeding may remove from memory spatial lo- wall, and each room had unique objects on the walls and 18 19 cation and other details of host nests that are no longer floor. The location of the baited food bowl differed be- 19 20 suitable for parasitizing and prepare the hippocampal tween rooms. We tested that birds could locate the cor- 20 21 memory system to process large numbers of new nests rect bowl in each room, which they did with 96% ac- 21 22 in the subsequent breeding season, nests that will have curacy, to confirm that they discriminated between the 22 23 many properties in common with each other and with rooms. In each room, another bowl was also randomly 23 24 nests of the previous season but also important distin- baited on each trial to encourage exploration and move- 24 25 guishing features such as location and the dynamic state ment and, thus, provide input for hypothesized spatially 25 26 of host clutch completion. responsive hippocampal neurons. All birds were trained 26 27 in both rooms. 27 28 28 CONTEXT-DEPENDENT CELLS IN On a final testing day birds had two 5-min trials in 29 29 the rooms separated by 25 min in their home cages. 30 THE BROWN-HEADED COWBIRD 30 Some birds experienced the same room twice in succes- 31 31 HIPPOCAMPUS sion while others experienced 2 different rooms. Con- 32 32 trol birds remained in their home cages. Within a few 33 The relatively large size of the hippocampus and the 33 minutes of completion of the second trial, birds were 34 occurrence of relatively greater levels of adult hippo- 34 sacrificed for visualization of Egr1 activation in the hip- 35 campal neurogenesis in the brown-headed cowbird sug- 35 pocampus using the method of cellular compartmen- 36 gest that the brown-headed cowbird hippocampus may 36 tal analysis of temporal fluorescence in situ hybridiza- 37 be specialized for the processing of spatial informa- 37 tion (catFISH). The catFISH method exploits the time 38 tion. If this is correct, then brown-headed cowbirds may 38 course of immediate early gene expression. Hippocam- 39 be a promising species in which to look for other neu- 39 pal neurons that were active in the second room only 40 ral traits associated with the processing of spatial infor- 40 should show Egr1 expression in the nucleus only, be- 41 mation. In mammals, there are a variety of cells dedicat- 41 cause sacrifice followed quickly after spatial exploration 42 ed to the processing of spatial information. Place cells 42 of the second room. Hippocampal neurons that were ac- 43 in the hippocampus, along with grid cells in the ento- 43 tive in the first room only should show Egr1 expression 44 rhinal cortex, and head direction cells in the entorhi- 44 in the cytoplasm only, because the time between neu- 45 nal cortex, presubiculum, thalamus and elsewhere in 45 ronal activity and sacrifice was long enough to allow 46 the mammalian brain act together to form an allocen- 46 Egr1 mRNA to move out of the nucleus into the cyto- 47 tric representation of space (Moser et al. 2008). The avi- 47 plasm. If hippocampal neurons were spatially respon- 48 an hippocampus also contains cells that are responsive 48 sive but did not discriminate the 2 spatial contexts of 49 to a bird’s spatial location. In the pigeon hippocampus 49 the rooms, most cells would have Egr1 in both nucleus 50 there are location cells that resemble place cells in some 50 and cytoplasm (Fig. 8). However, if hippocampal neu- 51 ways (Siegel et al. 2005), path cells (Siegel et al. 2006), 51

1 rons discriminated between the 2 spatial contexts, some The results showed that some hippocampal neurons 1 2 cells should show cytoplasmic activity only while others were, indeed, active only in the first spatial context (they 2 3 showed nuclear activity only. Egr1 activity in birds that had Egr1 only in the cytoplasm), others were active 3 4 experienced the same room twice in succession would only in the second spatial context (they had Egr1 only in 4 5 be expected to have both nuclear and cytoplasmic acti- the nucleus), and some were active in both (Fig. 9). Of 5 6 vation because the same hippocampal neurons respond- the cells that were active in both spatial contexts, sig- 6 7 ed twice in succession to the same spatial context (Grel- nificantly more were found in the hippocampus of birds 7 8 la et al. 2016). that explored the same room twice in succession com- 8 9 9 10 10 11 11 12 12 a b 13 13 14 14 15 15 16 16 17 17 18 18 19 19 20 20 21 21 22 22 23 23 24 24 25 25 26 Figure 8 (a) Confocal images of brown-headed cowbird hippocampal neuronal nuclei (blue DAPI). Some neurons show Egr1 26 27 mRNA expression (red) in the nucleus (arrowheads), while others show Egr1 mRNA in the cytoplasm (arrows). (b) Confocal imag- 27 28 es of hippocampal neurons with Egr1 mRNA expression in both the nucleus and the cytoplasm. 28 29 29 30 30 31 31 32 32 33 33 34 34 35 35 36 36 37 37 38 38 39 39 40 40 41 41 42 42 43 43 44 44 Figure 9 (a) Percent of hippocampal neurons with Egr1 expression following exposure to 2 spatial contexts. Epochs 1 and 2 refer 45 to the first and second room, respectively. Birds that explored the 2 rooms had significantly more Egr1 expression than birds that 45 46 remained in their home cages (black bars) whether they experienced the same room twice (white bars) or 2 different rooms (gray 46 47 bars). (b) Mean similarity scores show that hippocampal neurons that expressed Egr1 in response to both the first and second room 47 48 occurred more often when brown-headed cowbirds experienced the same room twice (white bar) than when they experienced 2 dif- 48 49 ferent rooms in succession (gray bars). The similarity score shows how many cells expressing Egr1 in Epoch 1 also expressed Egr1 49 50 in Epoch 2 and ranges from 0.0 indicating similarity due to chance to 1.0 indicating that all cells expressing Egr1 in Epoch 1 also 50 51 expressed Egr1 in Epoch 2. Asterisk and dagger indicate a significant difference,P < 0.05. 51

1 pared to birds that explored different rooms. These re- of brown-headed cowbirds contains spatially responsive 1 2 sults show that neurons in the brown-headed cowbird hippocampal neurons that may not only be involved in 2 3 hippocampus are, indeed, sensitive to spatial context representing the locations and other features of potential 3 4 and that different cells, possibly different networks of host nests but may also be the basis of spatial encoding 4 5 cells, respond to different spatial contexts. Place cells in in the avian hippocampus in general. 5 6 the rat hippocampus show this spatial context dependent 6 7 pattern of immediate early gene activity (Marrone et al. ACKNOWLEDGMENTS 7 8 2011). This does not prove that the cells we identified in 8 9 the brown-headed cowbird hippocampus are place cells. This research was supported by grants from the Natu- 9 10 Our experiment did not allow us to determine where in ral Sciences and Engineering Research Council of Can- 10 11 the rooms hippocampal neurons expressing Egr1 were ada, the Canada Foundation for Innovation, and the Re- 11 12 active and whether they had the spatial receptive fields search Development Office of Western University. 12 13 that characterize rat hippocampal place cells or pigeon 13 14 hippocampal location cells. Because the search task was USE OF ANIMALS IN RESEARCH 14 15 the same in both rooms, with equal reliance on memo- 15 16 ry for the baited food cup and comparable search among Original research described in this paper was con- 16 17 randomly baited food cups, and because the rooms were ducted following the Principles of Laboratory Ani- 17 18 approximately the same size, it is unlikely the differen- mal Care (NIH Publication Vol 25 No. 28 revised 1996; 18 19 tial activity of hippocampal neurons that we observed http://grants.nih.gov/grants/guide/notice-files/not96- 19 20 was task-dependent. It seems more likely that the differ- 208.html) and the guidelines of the Canadian Council 20 21 ential activity of neurons was the result of differential on Animal Care under Animal Use Protocol 2015-019 21 22 encoding of two different spatial contexts, but exactly approved by the Western University Animal Care Com- 22 23 how this occurs, and whether the cells we found corre- mittee. 23 24 spond to rodent place cells or location, path, pattern or 24 25 other cells found in the pigeon hippocampus remains to REFERENCES 25 26 be determined. 26 27 Aimone JB, Li Y, Lee SW, Clemenson GD, Deng W, 27 Gage FH (2014). Regulation and function of adult 28 CONCLUSIONS 28 29 neurogenesis: From genes to cognition. Physiological 29 30 The reproductive success of brood parasitic female Reviews 94, 991–1026. 30 31 brown-headed cowbirds depends on finding and remem- Astié AA, Kacelnik A, Reboreda JC (1998). Sexual dif- 31 32 bering potential host nests. After finding potential nests, ferences in memory in shiny cowbirds. Animal Cog- 32 33 females return to them to monitor host clutch comple- nition 1, 77–82. 33 34 tion, lay an egg, and sometimes remove a host egg. Astié AA, Scardamaglia RC, Muzio RN, Reboreda JC 34 35 Male brown-headed cowbirds do not search for host (2015). Sex differences in retention after a visual or a 35 36 nests. The outcome of this sex difference in spatial be- spatial discrimination learing task in brood parasitic 36 37 havior has been a suite of cognitive and neural adapta- shiny cowbirds. Behavioural Processes 119, 99–104. 37 38 tions for remembering the location and other properties Bruel-Jungerman E, Rampon C, Laroche S (2007). 38 39 of host nests. Females perform better than males on spa- Adult hippocampal neurogenesis, synaptic plastici- 39 40 tial tasks that resemble search for host nests but not on ty and memory: Facts and hypotheses. Reviews in the 40 41 another spatial task that does not. Female brown-head- Neurosciences 18, 93–114. 41 ed cowbirds possess a larger hippocampus than males, 42 Cameron HA, Glover LR (2015). Adult neurogenesis: 42 relative to the size of the telencephalon, although re- 43 Beyond learning and memory. Annual Review of Psy- 43 cent research shows this is a trait that may be shared 44 chology 66, 53–81. 44 45 with non-parasitic Icterids. Female brown-headed cow- 45 Clayton NS, Reboreda JC, Kacelnik A (1997). Season- 46 birds do show, however, greater hippocampal neurogen- 46 al changes of hippocampus volume in parasitic cow- 47 esis than males, a sex difference not found in non-par- 47 birds. Behavioral Processes 41, 237–43. 48 asitic relatives of brown-headed cowbirds. In addition, 48 49 hippocampal neurogenesis in brown-headed cowbirds is Davies NB (2000). Cuckoos, Cowbirds and Other 49 50 elevated following breeding, in contrast to the seasonal Cheats. T & A D Poyser, London. 50 51 pattern found in non-parasites. Finally, the hippocampus Deeming DC, Reynolds SJ, eds. (2016). Nests, eggs, 51

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