Defending Your Territory: It Pays To Have a Bigger Brain

Welcome to the second installment of Animal Territoriality Week. Today, we'll look at a case where differences in territory size can have implications for neuroanatomy. If you missed part 1 of Animal Territoriality week, check it out here.

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Let's say you have two very very closely related species. You might even call them congeneric, because they are from the same taxonomic genus. In most ways, these two species are very similar, but they differ behaviorally in some very big ways. Might those behavioral differences predict neurobiological differences?

The different species of the genus microtus display the full range of mammalian mating systems: some species are entirely monogamous, with two individuals mating for life, while other species are fully polygamous, with males having multiple female mates.

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Meet the monogamous pine vole (microtus pinetorum).

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Meet the polygamous meadow vole (microtus pennsylvanicus).

The difference in mating style leads to a very important difference in spatial memory requirements: for monogamous species, males and females both tend to live their lives in areas of land roughly the same size. For polygamous species, however, males' home ranges are much larger in spatial extent than the home range of the females (as well as the typical home ranges of the monogamous male voles). This makes sense: the polygamous male's home range needs to include the smaller home ranges of multiple female mates.

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On the left, a schematic diagram for the home ranges of monogamous voles. On the right, a schematic for the home ranges of polygamous voles. Solid pink blobs for females, dotted red lines for males.

Importantly, these behavioral differences in the polygamous voles are only seen in mature adults during mating season. Juvenile males voles of this species do not have significantly larger home ranges compared to females, and adults do not have larger home ranges during the rest of the year. These species and sex related differences probably create an important selective pressure for spatial memory.

The first question to ask is whether or not the observed sex and species differences in the spatial extent of the home range results in differences in spatial memory, as you might hypothesize. And the basic answer is yes: under laboratory conditions, voles of polygamous species show strong gender differences in tests of spatial ability, with males outperforming females. Voles of monogamous species fail to show these sex differences under identical testing conditions.

If the sexual selection for ranging behavior has influenced the evolution of cognition (at least with respect to spatial knowledge), then it is possible that it has also influenced the evolution of the parts of the brain known to subserve spatial navigation or spatial memory.

The hippocampus is known to play an important role in spatial learning. Rodents with hippocampal lesions show impaired performance on spatial tasks. In addition, the relative size of the hippocampus is larger in birds whose food-caching locations are located within a larger area, compared with other birds who use different food-caching strategies.

To test the hypothetical relationship between ranging behavior and hippocampal volume, the researchers went out and captured 40 wild voles during breeding season - 10 male and 10 female pine voles, and 10 male and 10 female meadow voles - and compared the size of the hippocampus between sexes for each species. (It would not make sense to directly compare the species, but it would make sense to compare the sex differences in hippocampus size between species.)

On average, the hippocampi of the polygamous male were 3.2 cubic millimeters larger than those of the females. For the monogamous voles, the males' hippocampi were only 0.5 cubic millimeters larger than the females. This aligns with the hypothesis, but comparing absolute differences between species and sexes isn't the proper comparison, since there are sex and species differences in total brain volume. When analyzing the ratio of hippocampal volume to total brain volume across sex and species, the differences remain statistically significant. The sex difference observed in the hippocampus volume in polygamous voles was significantly larger than that observed for the monogamous voles.

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Left, absolute values for hippocampal volume. Right, controlled for total brain volume. No difference for monogamous pine voles, but males hippocampi are significantly larger in polygamous meadow voles.

One principle of brain evolution that is intuitively appealing is that larger neural mass is related to increased information processing. However, it is hard to empirically test this principle, because it is difficult to isolate neural structures and then to assess their functions. However, this was one study that was able to successfully validate this principle, at least for one neural structure (the hippocampus) which has repeatedly been shown to be involved the processing of a specific type of information (spatial processing), in two different vole species..

It is important to note that on the basis of these findings, it is not possible to conclusively determine whether or not the observed sex differences are determined biologically or if they experience results in larger hippocampi. Only a controlled laboratory study could address this question. However, the selective pressure created by mating style on spatial abilities, and the subsequent neurobiological differences observed, seem fairly well supported. The authors point out, and rightly so, that the presence or absence of potential effects of experience does not necessarily preclude an evolutionary explanation for the sex differences that they observed.

So, if you learned only one thing today: polygamous male voles have larger hippocampi which allows them to maintain their larger territories, compared with monogamous males.

Jacobs, L. (1990). Evolution of Spatial Cognition: Sex-Specific Patterns of Spatial Behavior Predict Hippocampal Size Proceedings of the National Academy of Sciences, 87 (16), 6349-6352. DOI: 10.1073/pnas.87.16.6349

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