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Tsuboi, M., Lim, A. C., Ooi, B. L., Yip, M. Y., Chong, V. C., Ahnesjö, I. & Kolm, N. (2017). Brain size evolution in pipefishes and seahorses: the role of feeding ecology, life history and sexual selection. Journal of Evolutionary Biology, 30(1), 150-160
Open this publication in new window or tab >>Brain size evolution in pipefishes and seahorses: the role of feeding ecology, life history and sexual selection
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2017 (English)In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 30, no 1, p. 150-160Article in journal (Refereed) Published
Abstract [en]

Brain size varies greatly at all taxonomic levels. Feeding ecology, life history and sexual selection have been proposed as key components in generating contemporary diversity in brain size across vertebrates. Analyses of brain size evolution have, however, been limited to lineages where males predominantly compete for mating and females choose mates. Here, we present the first original data set of brain sizes in pipefishes and seahorses (Syngnathidae) a group in which intense female mating competition occurs in many species. After controlling for the effect of shared ancestry and overall body size, brain size was positively correlated with relative snout length. Moreover, we found that females, on average, had 4.3% heavier brains than males and that polyandrous species demonstrated more pronounced (11.7%) female-biased brain size dimorphism. Our results suggest that adaptations for feeding on mobile prey items and sexual selection in females are important factors in brain size evolution of pipefishes and seahorses. Most importantly, our study supports the idea that sexual selection plays a major role in brain size evolution, regardless of on which sex sexual selection acts stronger.

Keywords
brain evolution, phylogenetic comparative analysis, pipefishes & seahorses, sexual selection & conflicts
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-320072 (URN)10.1111/jeb.12995 (DOI)000394852200012 ()27748990 (PubMedID)
Funder
Helge Ax:son Johnsons stiftelse Swedish Research Council, 621-2012-3624
Available from: 2017-04-13 Created: 2017-04-13 Last updated: 2017-05-03Bibliographically approved
Hayward, A., Tsuboi, M., Owusu, C. K., Kotrschal, A., Buechel, S. D., Zidar, J., . . . Kolm, N. (2017). Evolutionary associations between host traits and parasite load: insights from Lake Tanganyika cichlids. Journal of Evolutionary Biology, 30(6), 1056-1067
Open this publication in new window or tab >>Evolutionary associations between host traits and parasite load: insights from Lake Tanganyika cichlids
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2017 (English)In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 30, no 6, p. 1056-1067Article in journal (Refereed) Published
Abstract [en]

Parasite diversity and abundance (parasite load) vary greatly among host species. However, the influence of host traits on variation in parasitism remains poorly understood. Comparative studies of parasite load have largely examined measures of parasite species richness and are predominantly based on records obtained from published data. Consequently, little is known about the relationships between host traits and other aspects of parasite load, such as parasite abundance, prevalence and aggregation. Meanwhile, understanding of parasite species richness may be clouded by limitations associated with data collation from multiple independent sources. We conducted a field study of Lake Tanganyika cichlid fishes and their helminth parasites. Using a Bayesian phylogenetic comparative framework, we tested evolutionary associations between five key host traits (body size, gut length, diet breadth, habitat complexity and number of sympatric hosts) predicted to influence parasitism, together with multiple measures of parasite load. We find that the number of host species that a particular host may encounter due to its habitat preferences emerges as a factor of general importance for parasite diversity, abundance and prevalence, but not parasite aggregation. In contrast, body size and gut size are positively related to aspects of parasite load within, but not between species. The influence of host phylogeny varies considerably among measures of parasite load, with the greatest influence exerted on parasite diversity. These results reveal that both host morphology and biotic interactions are key determinants of host-parasite associations and that consideration of multiple aspects of parasite load is required to fully understand patterns in parasitism.

Place, publisher, year, edition, pages
WILEY, 2017
Keywords
endoparasite, evolution, fish, helminth, parasitic worm
National Category
Evolutionary Biology Ecology
Identifiers
urn:nbn:se:uu:diva-328154 (URN)10.1111/jeb.13053 (DOI)000403155000001 ()28187238 (PubMedID)
Funder
Swedish Research CouncilHelge Ax:son Johnsons stiftelse Göran Gustafsson Foundation for Research in Natural Sciences and Medicine
Available from: 2018-02-20 Created: 2018-02-20 Last updated: 2018-02-20Bibliographically approved
Tsuboi, M., Kotrschal, A., Hayward, A., Buechel, S., Zidar, J., Løvlie, H. & Kolm, N. (2016). Evolution of brain-body allometry in Lake Tanganyika cichlids. Evolution, 70(7), 1559-1568
Open this publication in new window or tab >>Evolution of brain-body allometry in Lake Tanganyika cichlids
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2016 (English)In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 70, no 7, p. 1559-1568Article in journal (Refereed) Published
Abstract [en]

Brain size is strongly associated with body size at all taxonomic levels. This relationship has been hypothesized to be an important constraint on adaptive brain size evolution. The essential assumption of this idea is that allometry has a limited ability to evolve, and that evolution of relative brain size is therefore constrained to occur along the direction of static (i.e. within species) allometry. However, recent studies have reported mixed support for this view. Here, we examine if static allometry has affected the rate of relative brain size evolution in Lake Tanganyika cichlids. The evolution of brain-body allometry showed a recent rapid divergence whereas brain size evolution represented a more gradual phenotypic divergence across the history of diversification. Accordingly, we found no support for that static allometry affected the rate of absolute or relative brain size evolution in this group. Instead, we detected low, but existing evolvability of static allometry. Moreover, static allometry evolved faster in species with relatively small and large brains than in species with medium brain size. We propose that a combination of allometric constraints and partial evolvability of static allometry have allowed for independent evolution of brain size in Lake Tanganyika cichlids. Overall, our results demonstrate a complex, yet important, role of brain-body allometry in brain size evolution. 

National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-262069 (URN)10.1111/evo.12965 (DOI)000380023200011 ()27241216 (PubMedID)
External cooperation:
Funder
Helge Ax:son Johnsons stiftelse Swedish Research Council, 621-2012-3624
Note

Title in Thesis list of papers: Brain size evolution under allometric constraints in Lake Tanganyika cichlids

Available from: 2015-09-08 Created: 2015-09-08 Last updated: 2018-06-26Bibliographically approved
Tsuboi, M., Husby, A., Kotrschal, A., Hayward, A., Buechel, S. D., Zidar, J., . . . Kolm, N. (2015). Comparative support for the expensive tissue hypothesis: Big brains are correlated with smaller gut and greater parental investment in Lake Tanganyika cichlids. Evolution, 69(1), 190-200
Open this publication in new window or tab >>Comparative support for the expensive tissue hypothesis: Big brains are correlated with smaller gut and greater parental investment in Lake Tanganyika cichlids
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2015 (English)In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 69, no 1, p. 190-200Article in journal (Refereed) Published
Abstract [en]

The brain is one of the most energetically expensive organs in the vertebrate body. Consequently, the energetic requirements of encephalization are suggested to impose considerable constraints on brain size evolution. Three main hypotheses concerning how energetic constraints might affect brain evolution predict covariation between brain investment and (1) investment into other costly tissues, (2) overall metabolic rate, and (3) reproductive investment. To date, these hypotheses have mainly been tested in homeothermic animals and the existing data are inconclusive. However, there are good reasons to believe that energetic limitations might play a role in large-scale patterns of brain size evolution also in ectothermic vertebrates. Here, we test these hypotheses in a group of ectothermic vertebrates, the Lake Tanganyika cichlid fishes. After controlling for the effect of shared ancestry and confounding ecological variables, we find a negative association between brain size and gut size. Furthermore, we find that the evolution of a larger brain is accompanied by increased reproductive investment into egg size and parental care. Our results indicate that the energetic costs of encephalization may be an important general factor involved in the evolution of brain size also in ectothermic vertebrates.

Keywords
Brain evolution, constraints, encephalization, phylogenetic comparative methods, the expensive tissue hypothesis, trade-offs
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-243668 (URN)10.1111/evo.12556 (DOI)000347462800015 ()25346264 (PubMedID)
Available from: 2015-02-20 Created: 2015-02-11 Last updated: 2017-12-04Bibliographically approved
Tsuboi, M., Gonzalez-Voyer, A. & Kolm, N. (2015). Functional coupling constrains craniofacial diversification in Lake Tanganyika cichlids. Biology Letters, 11(5), Article ID 20141053.
Open this publication in new window or tab >>Functional coupling constrains craniofacial diversification in Lake Tanganyika cichlids
2015 (English)In: Biology Letters, ISSN 1744-9561, E-ISSN 1744-957X, Vol. 11, no 5, article id 20141053Article in journal (Refereed) Published
Abstract [en]

Functional coupling, where a singlemorphological trait performs multiple functions, is a universal feature of organismal design. Theory suggests that functional coupling may constrain the rate of phenotypic evolution, yet empirical tests of this hypothesis are rare. In fish, the evolutionary transition from guarding the eggs on a sandy/rocky substrate (i.e. substrate guarding) to mouthbrooding introduces a novel function to the craniofacial system and offers an ideal opportunity to test the functional coupling hypothesis. Using a combination of geometric morphometrics and a recently developed phylogenetic comparative method, we found that head morphology evolution was 43% faster in substrate guarding species than in mouthbrooding species. Furthermore, for species in which females were solely responsible for mouthbrooding the males had a higher rate of head morphology evolution than in those with biparental mouthbrooding. Our results support the hypothesis that adaptations resulting in functional coupling constrain phenotypic evolution.

Keywords
functional coupling, constraints, phylogenetic comparative analysis, geometric morphometrics, rate of evolution
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-260156 (URN)10.1098/rsbl.2014.1053 (DOI)000357684200003 ()25948565 (PubMedID)
Available from: 2015-08-17 Created: 2015-08-17 Last updated: 2017-12-04Bibliographically approved
Tsuboi, M. (2015). Thinking in water: Brain size evolution in Cichlidae and Syngnathidae. (Doctoral dissertation). Uppsala: Acta Universitatis Upsaliensis
Open this publication in new window or tab >>Thinking in water: Brain size evolution in Cichlidae and Syngnathidae
2015 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Brain size varies greatly among vertebrates. It has been proposed that the diversity of brain size is produced and maintained through a balance of adaptations to different types and levels of cognitive ability and constraints for adaptive evolution. Phylogenetic comparative studies have made major contributions to our understanding of brain size evolution. However, previous studies have nearly exclusively focused on mammalian and avian taxa and almost no attempts have been made to investigate brain size evolution in ectothermic vertebrates.

In my thesis, I studied brain size evolution in two groups of fish with extreme diversity in ecology, morphology and life history, Cichlidae and Syngnathidae. Using phylogenetic comparative methods, I investigated four key questions in vertebrate brain size evolution; cognitive adaptation, sexual selection, phenotypic integration and energetic constraints.

I have demonstrated i) that phenotypic integration can link functionally unrelated traits, and this may constrain independent evolution of each part involved or promote concerted evolution of an integrated whole, ii) that brain-body static allometry constrains the direction of brain size evolution, even though the static-allometry showed ability to evolve, allowing evolution of relative brain size under allometric constraints, iii) that the energetic constraints of development and maintenance of brain tissue is an important factor in forming the diversity in brain size in cichlids and syngnathids, both at macroevolutionary and microevolutionary time scales, and iv) that adaptation for feeding and female mating competition may have played key roles in the adaptive evolution of brain size in pipefishes and seahorses. To conclude, my thesis shows the strong benefit of using fish as a model system to study brain size evolution with a phylogenetic comparative framework.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2015. p. 50
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1286
Keywords
brain evolution, phylogenetic comparative method, the expensive tissue hypothesis, cichlid, pipefish, seahorse
National Category
Evolutionary Biology
Research subject
Biology with specialization in Animal Ecology
Identifiers
urn:nbn:se:uu:diva-262216 (URN)978-91-554-9333-2 (ISBN)
Public defence
2015-10-29, Zootissalen, Villavägen 9, tr.2, Uppsala, 10:15 (English)
Opponent
Supervisors
Available from: 2015-10-07 Created: 2015-09-10 Last updated: 2018-06-26
Tsuboi, M., Gonzalez-Voyer, A. & Kolm, N. (2014). Phenotypic integration of brain size and head morphology in Lake Tanganyika Cichlids. BMC Evolutionary Biology, 14, 39
Open this publication in new window or tab >>Phenotypic integration of brain size and head morphology in Lake Tanganyika Cichlids
2014 (English)In: BMC Evolutionary Biology, ISSN 1471-2148, E-ISSN 1471-2148, Vol. 14, p. 39-Article in journal (Refereed) Published
Abstract [en]

Background: Phenotypic integration among different anatomical parts of the head is a common phenomenon across vertebrates. Interestingly, despite centuries of research into the factors that contribute to the existing variation in brain size among vertebrates, little is known about the role of phenotypic integration in brain size diversification. Here we used geometric morphometrics on the morphologically diverse Tanganyikan cichlids to investigate phenotypic integration across key morphological aspects of the head. Then, while taking the effect of shared ancestry into account, we tested if head shape was associated with brain size while controlling for the potentially confounding effect of feeding strategy. Results: The shapes of the anterior and posterior parts of the head were strongly correlated, indicating that the head represents an integrated morphological unit in Lake Tanganyika cichlids. After controlling for phylogenetic non-independence, we also found evolutionary associations between head shape, brain size and feeding ecology. Conclusions: Geometric morphometrics and phylogenetic comparative analyses revealed that the anterior and posterior parts of the head are integrated, and that head morphology is associated with brain size and feeding ecology in Tanganyikan cichlid fishes. In light of previous results on mammals, our results suggest that the influence of phenotypic integration on brain diversification is a general process.

Keywords
Phenotypic integration, Geometric morphometrics, Phylogenetic comparative analysis, Lake Tanganyika cichlid, Brain evolution, Constraints
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-225106 (URN)10.1186/1471-2148-14-39 (DOI)000334458900001 ()
Available from: 2014-05-27 Created: 2014-05-27 Last updated: 2017-12-05Bibliographically approved
Tsuboi, M., Gonzalez-Voyer, A., Höglund, J. & Kolm, N. (2012). Ecology and mating competition influence sexual dimorphism in Tanganyikan cichlids. Evolutionary Ecology, 26(1), 171-185
Open this publication in new window or tab >>Ecology and mating competition influence sexual dimorphism in Tanganyikan cichlids
2012 (English)In: Evolutionary Ecology, ISSN 0269-7653, E-ISSN 1573-8477, Vol. 26, no 1, p. 171-185Article in journal (Refereed) Published
Abstract [en]

Sexual selection contributes strongly to the evolution of sexual dimorphism among animal taxa. However, recent comparative analyses have shown that evolution of sexual dimorphism can be influenced by extrinsic factors like mating system and environment, and also that different types of sexual dimorphism may present distinct evolutionary pathways. Investigating the co-variation among different types of sexual dimorphism and their association with environmental factors can therefore provide important information about the mechanisms generating variation in sexual dimorphism among contemporary species. Using phylogenetic comparative analyses comparing 49 species of Tanganyikan cichlid fishes, we first investigated the pairwise relationship between three types of sexual dimorphism [size dimorphism (SSD), colour dimorphism (COD) and shape dimorphism (SHD)] and how they were related to the strength of pre- and post-copulatory sexual selection. We then investigated the influence of ecological features on sexual dimorphism. Our results showed that although SSD was associated with the overall strength of sexual selection it was not related to other types of sexual dimorphism. Also, SSD co-varied with female size and spawning habitat, suggesting a role for female adaptations to spawn in small crevices and shells influencing SSD in this group. Further, COD and SHD were positively associated and both show positive relationships with the strength of sexual selection. Finally, the level of COD and SHD was related to habitat complexity. Our results thus highlight distinct evolutionary pathways for different types of sexual dimorphism and further that ecological factors have influenced the evolution of sexual dimorphism in Tanganyikan cichlid fishes.

Keywords
Sexual dimorphism, Phylogenetic principal component analysis, Habitat, Diet, Depth, Adaptive radiation
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-167172 (URN)10.1007/s10682-011-9489-3 (DOI)000298105900013 ()
Available from: 2012-01-25 Created: 2012-01-23 Last updated: 2017-12-08Bibliographically approved
Tsuboi, M., Lim, A. C., Ooi, B. L., Mei, Y. Y., Chong, V. C., Ahnesjö, I. & Kolm, N.Prey motility, egg size and female mating competition: brain size evolution in pipefishes and seahorses.
Open this publication in new window or tab >>Prey motility, egg size and female mating competition: brain size evolution in pipefishes and seahorses
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

Brain size varies greatly at all taxonomic levels. Feeding ecology, life history and sexual selection have been proposed as key components in generating the existing contemporary diversity in brain size across vertebrates. Analyses of brain size evolution have, however, been limited to lineages where males predominantly compete for mating and females choose mates. Here, we present the first original data set of brain sizes in pipefishes and seahorses (Syngnathidae). In this group, intense female mating competition occurs in many species (i.e. reversed sex-roles), and mating patterns include monogamy, polygynandry and polyandry. After controlling for the effect of shared ancestry and overall body size, relatively larger brains were positively correlated with relatively longer snout length, which is related to the propensity for feeding on motile and evasive prey items in Syngnathidae, and larger egg size. Furthermore, we found that females, on average, had 4.3% heavier brains than males and that polyandrous species tended to demonstrate female-favored brain size dimorphism. Our results suggest that adaptations for feeding on motile prey items, energetic constraints associated with production of large-brained juveniles and sexual selection in females are important factors in brain size evolution of pipefishes and seahorses.

Keywords
Brain size evolution, Phylogenetic comparative methods, Syngnathidae
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-262073 (URN)
Available from: 2015-09-08 Created: 2015-09-08 Last updated: 2018-06-26
Tsuboi, M., Shoji, J., Sogabe, A., Ahnesjö, I. & Kolm, N.Within species support for the expensive tissue hypothesis: a negative association between brain size and visceral fat storage in females of Pacific seaweed pipefish.
Open this publication in new window or tab >>Within species support for the expensive tissue hypothesis: a negative association between brain size and visceral fat storage in females of Pacific seaweed pipefish
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

The brain is one of the most energetically expensive organs in the vertebrate body. Consequently, the high cost of brain development and maintenance is predicted to constrain adaptive brain size evolution (the expensive tissue hypothesis, ETH). Here, we test the ETH in a teleost fish with predominant female mating competition (reversed sex-roles) and male pregnancy, the pacific seaweed pipefish Syngnathus schlegeli. The relative size of the brain and other energetically expensive organs (kidney, liver, heart, gut, visceral fat, ovary/testis) was compared among three groups: pregnant males, non-pregnant males and egg producing females. Brood size in pregnant males was unrelated to brain size or the size of any other organ, whereas positive relationships were found between ovary size, kidney size and liver size in females. Moreover, we found that the size a suite of energetically expensive organs (brain, heart, gut, kidney, liver) as well as the amount of visceral fat did not differ between pregnant and non-pregnant males. However, we found marked differences in relative size of the expensive organs between sexes. Females had larger liver and kidney than males, whereas males stored more visceral fat than females. Furthermore, in females we found a negative correlation between brain size and the amount of visceral fat, whereas in males a positive trend between brain size and both liver and heart size was found. These results suggest that, while the majority of variation in the size of various expensive organs in this species likely reflects that individuals in good condition can afford to allocate resources to several organs, the cost of the expensive brain was visible in the visceral fat content of females, possibly due to the high costs associated with female egg production. 

Keywords
The expensive tissue hypothesis, Brain size evolution, pipefish
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-262071 (URN)
Available from: 2015-09-08 Created: 2015-09-08 Last updated: 2018-06-26
Organisations
Identifiers
ORCID iD: ORCID iD iconorcid.org/0000-0002-0144-2893

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