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A larger brain confers a benefit in a spatial mate search learning task in male guppies.

Kotrschal A, Corral-Lopez A, Amcoff M, Kolm N - Behav. Ecol. (2014)

Bottom Line: However, experimental evidence for the link between relative brain size and cognitive ability is surprisingly scarce and to date stems from a single study on brain size selected guppies (Poecilia reticulata), where large-brained females were shown to outperform small-brained females in a numerical learning assay.Because the results were inconclusive for males in that study, we here use a more ecologically relevant test of male cognitive ability to investigate whether or not a relatively larger brain increases cognitive ability also in males.Our results support that relatively larger brains are better also for males in some contexts, which further substantiates that variation in vertebrate brain size is generated through the balance between energetic costs and cognitive benefits.

View Article: PubMed Central - PubMed

Affiliation: Department of Animal Ecology, Evolutionary Biology Centre, Uppsala University , Norbyvägen 18D, SE-75236 Uppsala , Sweden and ; Department of Zoology/Ethology, Stockholm University , Svante Arrheniusväg 18 B, SE-10691 Stockholm , Sweden.

ABSTRACT

Brain size varies dramatically among vertebrates, and selection for increased cognitive abilities is thought to be the key force underlying the evolution of a large brain. Indeed, numerous comparative studies suggest positive relationships between cognitively demanding aspects of behavior and brain size controlled for body size. However, experimental evidence for the link between relative brain size and cognitive ability is surprisingly scarce and to date stems from a single study on brain size selected guppies (Poecilia reticulata), where large-brained females were shown to outperform small-brained females in a numerical learning assay. Because the results were inconclusive for males in that study, we here use a more ecologically relevant test of male cognitive ability to investigate whether or not a relatively larger brain increases cognitive ability also in males. We compared mate search ability of these artificially selected large- and small-brained males in a maze and found that large-brained males were faster at learning to find a female in a maze. Large-brained males decreased the time spent navigating the maze faster than small-brained males and were nearly twice as fast through the maze after 2 weeks of training. Our results support that relatively larger brains are better also for males in some contexts, which further substantiates that variation in vertebrate brain size is generated through the balance between energetic costs and cognitive benefits.

No MeSH data available.


Maze setup used to determine the decrease in search time in male guppies artificially selected for large and small relative brain size. Males were placed in a clear Perspex ring (a); after the ring was remotely lifted, the fish were free to explore the maze. On arrival in the end compartment (b), the clear Perspex ring around the female (c) was remotely lifted. The maze is to scale (scale bar represents 10cm) while fish are depicted approximately 5 times larger.
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Figure 1: Maze setup used to determine the decrease in search time in male guppies artificially selected for large and small relative brain size. Males were placed in a clear Perspex ring (a); after the ring was remotely lifted, the fish were free to explore the maze. On arrival in the end compartment (b), the clear Perspex ring around the female (c) was remotely lifted. The maze is to scale (scale bar represents 10cm) while fish are depicted approximately 5 times larger.

Mentions: In order to test whether relatively larger brains confer a cognitive advantage for male guppies, we assessed their ability to decrease the time spent navigating a maze using an associative learning regime with access to a female as reward at the end of the maze. As explained above, spatial cognition should be a highly relevant cognitive trait in male guppies (Croft et al. 2003). Groups of females have smaller home ranges and are repeatedly visited by males (Houde 1997). Our setup mimicked this situation in which males need to navigate through shallow water in the search of females. The maze was constructed of a 100×30cm tank with opaque walls, the bottom was covered by fine gravel and the water depth was 10cm. The maze also contained 2 dead-end areas to increase the level of difficulty and counteract potential biases from differences in overall swimming activity levels (Figure 1). Once per day, each fish was placed into a clear Perspex ring (Figure 1a) at one end of the maze. After a 1-min acclimation period, the ring was lifted and the time until the fish left the start compartment was recorded (“latency” from hereon). Next, the time until the fish had reached the end compartment was recorded (“search time” from hereon, Figure 1b). On arrival of the focal male in the final compartment, another clear Perspex ring was remotely lifted (Figure 1c), which released a “receptive” female as a reward (see below). The direct line distance from start to finish was 100cm. Average critical swimming speed (the maximal speed animals can swim with for extended periods of time) for males of this population of guppies is 13cm/s (Lievens 2012). Individuals swimming on the shortest path should, therefore, be able to complete the maze within 100/13 = 7.7 s. After completion of the maze, the male and female were allowed to interact for 3min. If the focal male did not complete the maze within 8min, it was gently guided through the maze with a hand net. To ensure the potential for positive associative learning also for the males that did not complete the maze by themselves, they were also rewarded with access to the female, but they were treated as missing values during analyses. The order of males during the day was random with regard to brain size. We kept the sequence during the experiment to ensure a constant time period of approximately 24h until the same individual was retested. Female guppies actively solicit copulations when they are receptive, and female guppies are normally receptive when they are virgin, recently mated (up to 5 days), or in a postpartum phase (Guevara-Fiore et al. 2009). We used a total of 28 virgin females, from an unselected base population, and these females were changed twice per day to maintain their receptive status. The procedure was repeated for 14 consecutive days because guppies from high-predation populations have been shown to learn the way through a simple maze within 2 weeks (Burns and Rodd 2008), and the origin of the here used animals is a high-predation site (Kotrschal et al. 2013a). Failure to reach the female within the 8-min period was only observed during the first 3 days and for a limited number of males (day 1: 6 large-brained and 6 small-brained individuals, day 2: 6 large-brained and 6 small-brained individuals, and day 3: 2 large-brained and 3 small-brained individuals). This almost identical number of large- and small-brained males not finishing the maze within the 8-min period means that exclusion of those males is unlikely to have created a systematic bias in our results.


A larger brain confers a benefit in a spatial mate search learning task in male guppies.

Kotrschal A, Corral-Lopez A, Amcoff M, Kolm N - Behav. Ecol. (2014)

Maze setup used to determine the decrease in search time in male guppies artificially selected for large and small relative brain size. Males were placed in a clear Perspex ring (a); after the ring was remotely lifted, the fish were free to explore the maze. On arrival in the end compartment (b), the clear Perspex ring around the female (c) was remotely lifted. The maze is to scale (scale bar represents 10cm) while fish are depicted approximately 5 times larger.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4374130&req=5

Figure 1: Maze setup used to determine the decrease in search time in male guppies artificially selected for large and small relative brain size. Males were placed in a clear Perspex ring (a); after the ring was remotely lifted, the fish were free to explore the maze. On arrival in the end compartment (b), the clear Perspex ring around the female (c) was remotely lifted. The maze is to scale (scale bar represents 10cm) while fish are depicted approximately 5 times larger.
Mentions: In order to test whether relatively larger brains confer a cognitive advantage for male guppies, we assessed their ability to decrease the time spent navigating a maze using an associative learning regime with access to a female as reward at the end of the maze. As explained above, spatial cognition should be a highly relevant cognitive trait in male guppies (Croft et al. 2003). Groups of females have smaller home ranges and are repeatedly visited by males (Houde 1997). Our setup mimicked this situation in which males need to navigate through shallow water in the search of females. The maze was constructed of a 100×30cm tank with opaque walls, the bottom was covered by fine gravel and the water depth was 10cm. The maze also contained 2 dead-end areas to increase the level of difficulty and counteract potential biases from differences in overall swimming activity levels (Figure 1). Once per day, each fish was placed into a clear Perspex ring (Figure 1a) at one end of the maze. After a 1-min acclimation period, the ring was lifted and the time until the fish left the start compartment was recorded (“latency” from hereon). Next, the time until the fish had reached the end compartment was recorded (“search time” from hereon, Figure 1b). On arrival of the focal male in the final compartment, another clear Perspex ring was remotely lifted (Figure 1c), which released a “receptive” female as a reward (see below). The direct line distance from start to finish was 100cm. Average critical swimming speed (the maximal speed animals can swim with for extended periods of time) for males of this population of guppies is 13cm/s (Lievens 2012). Individuals swimming on the shortest path should, therefore, be able to complete the maze within 100/13 = 7.7 s. After completion of the maze, the male and female were allowed to interact for 3min. If the focal male did not complete the maze within 8min, it was gently guided through the maze with a hand net. To ensure the potential for positive associative learning also for the males that did not complete the maze by themselves, they were also rewarded with access to the female, but they were treated as missing values during analyses. The order of males during the day was random with regard to brain size. We kept the sequence during the experiment to ensure a constant time period of approximately 24h until the same individual was retested. Female guppies actively solicit copulations when they are receptive, and female guppies are normally receptive when they are virgin, recently mated (up to 5 days), or in a postpartum phase (Guevara-Fiore et al. 2009). We used a total of 28 virgin females, from an unselected base population, and these females were changed twice per day to maintain their receptive status. The procedure was repeated for 14 consecutive days because guppies from high-predation populations have been shown to learn the way through a simple maze within 2 weeks (Burns and Rodd 2008), and the origin of the here used animals is a high-predation site (Kotrschal et al. 2013a). Failure to reach the female within the 8-min period was only observed during the first 3 days and for a limited number of males (day 1: 6 large-brained and 6 small-brained individuals, day 2: 6 large-brained and 6 small-brained individuals, and day 3: 2 large-brained and 3 small-brained individuals). This almost identical number of large- and small-brained males not finishing the maze within the 8-min period means that exclusion of those males is unlikely to have created a systematic bias in our results.

Bottom Line: However, experimental evidence for the link between relative brain size and cognitive ability is surprisingly scarce and to date stems from a single study on brain size selected guppies (Poecilia reticulata), where large-brained females were shown to outperform small-brained females in a numerical learning assay.Because the results were inconclusive for males in that study, we here use a more ecologically relevant test of male cognitive ability to investigate whether or not a relatively larger brain increases cognitive ability also in males.Our results support that relatively larger brains are better also for males in some contexts, which further substantiates that variation in vertebrate brain size is generated through the balance between energetic costs and cognitive benefits.

View Article: PubMed Central - PubMed

Affiliation: Department of Animal Ecology, Evolutionary Biology Centre, Uppsala University , Norbyvägen 18D, SE-75236 Uppsala , Sweden and ; Department of Zoology/Ethology, Stockholm University , Svante Arrheniusväg 18 B, SE-10691 Stockholm , Sweden.

ABSTRACT

Brain size varies dramatically among vertebrates, and selection for increased cognitive abilities is thought to be the key force underlying the evolution of a large brain. Indeed, numerous comparative studies suggest positive relationships between cognitively demanding aspects of behavior and brain size controlled for body size. However, experimental evidence for the link between relative brain size and cognitive ability is surprisingly scarce and to date stems from a single study on brain size selected guppies (Poecilia reticulata), where large-brained females were shown to outperform small-brained females in a numerical learning assay. Because the results were inconclusive for males in that study, we here use a more ecologically relevant test of male cognitive ability to investigate whether or not a relatively larger brain increases cognitive ability also in males. We compared mate search ability of these artificially selected large- and small-brained males in a maze and found that large-brained males were faster at learning to find a female in a maze. Large-brained males decreased the time spent navigating the maze faster than small-brained males and were nearly twice as fast through the maze after 2 weeks of training. Our results support that relatively larger brains are better also for males in some contexts, which further substantiates that variation in vertebrate brain size is generated through the balance between energetic costs and cognitive benefits.

No MeSH data available.