The mating brain: early maturing sneaker males maintain investment into the brain also under fast body growth in Atlantic salmon (Salmo salar)
Alexander Kotrschal
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Susanne Trombley
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Bjo rn Rogell
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Ioana Brannstro m
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Eric Foconi
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Monika Schmitz
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Niclas Kolm
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B. Rogell School of Biological Sciences, Monash University
, Clayton,
VIC 3800, Australia
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S. Trombley M. Schmitz Department of Organismal Biology, Comparative Physiology, Evolutionary Biology Centre, Uppsala University
, Norbyvagen 18A, 75236 Uppsala,
Sweden
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A. Kotrschal Department for Integrative Biology and Evolution (KLIVV), Veterinary University Vienna
, Savoyenstrasse 1A,
1160 Vienna, Austria
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N. Kolm Department of Zoology/Ethology, Stockholm University
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10691 Stockholm, Sweden
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I. Brannstrom Department of Ecology and Genetics, Evolutionary Biology Centre, Uppsala University
, Norbyvagen 18D, 75236 Uppsala,
Sweden
It has been suggested that mating behaviours require high levels of cognitive ability. However, since investment into mating and the brain both are costly features, their relationship is likely characterized by energetic trade-offs. Empirical data on the subject remains equivocal. We investigated if early sexual maturation was associated with brain development in Atlantic salmon (Salmo salar), in which males can either stay in the river and sexually mature at a small size (sneaker males) or migrate to the sea and delay sexual maturation until they have grown much larger (anadromous males). Specifically, we tested how sexual maturation may induce plastic changes in brain development by rearing juveniles on either natural or ad libitum feeding levels. After their first season we
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compared brain size and brain region volumes across both types of male mating tactics and
females. Body growth increased greatly across both male mating tactics and females during
ad libitum feeding as compared to natural feeding levels. However, despite similar relative
increases in body size, early maturing sneaker males maintained larger relative brain size
during ad libitum feeding levels as compared to anadromous males and females. We also
detected several differences in the relative size of separate brain regions across feeding
treatments, sexes and mating strategies. For instance, the relative size of the cognitive
centre of the brain, the telencephalon, was largest in sneaker males. Our data support that a
large relative brain size is maintained in individuals that start reproduction early also
during fast body growth. We propose that the cognitive demands during complex mating
behaviours maintain a high level of investment into brain development in reproducing
individuals.
Sneaker Salmo
Brain morphology is highly variable at all taxonomic levels among vertebrates (Jerison 1973;
Kotrschal et al. 2013) and explaining this variation continues to be an important question in
modern evolutionary biology (Striedter 2005). Theory and empirical data maintain that brain
morphology evolves under the balance between positive selection for cognitive ability and
the energetic costs of maintaining a larger and more complex brain (Aiello and Wheeler 1995;
Darwin 1871; Isler and van Schaik 2006; Jacobs 1996; Jerison 1973; Kotrschal et al. 2013).
Comparative analyses and recent experimental data have found support for cognitive benefits
of increased relative brain size (Kotrschal et al. 2013), increased neuron density (Haug 1987)
and increased size of specific brain regions (Maguire et al. 2006). We adhere to the broad
definition of cognition as comprising all mechanisms that invertebrates and vertebrates
have for taking in information through their senses, retaining it, and using it to adjust
behaviour to local conditions (Shettleworth 2010). At the same time, given the energetically
costly nature of the vertebrate brain, trade-offs between investment into the brain and other
costly features of an organisms biology have long been assumed to be important in
generating variation in brain morphology (Aiello and Wheeler 1995; Boogert et al. 2011; Kotrschal
et al. 2013; Navarrete et al. 2011; Striedter 2005). Interestingly, despite many decades of
interest in the selection pressures for increased brain size and potential trade-offs,
experimental data are still scarce regarding the selection pressures that affect brain complexity.
A key-aspect of any organisms life history is reproduction (Roff 1992). Reproduction is
also interesting from the perspective of brain evolution and development since it may
assert selection for both increases and decreases in brain size. It has been proposed that
cognitive ability is highly important during courtship, mating and parental care (Boogert
et al. 2011; Gittleman 1994; Gonzalez-Voyer et al. 2009b; Jacobs 1996; Jacobs et al.
1990). Hence, the requirement of complex behaviours associated with reproduction could
select on increased brain size or complexity. At the same time, reproduction is a highly
costly feature in any organism (Harshman and Zera 2007; Roff 1992; Williams 1966) and
could therefore place i (...truncated)