The astonishing diversity of brain sizes observed across the animal kingdom is typically explained in the context of trade-offs: the benefits of a larger brain, such as enhanced cognitive ability, are balanced against potential costs, such as increased energetic demands. Several hypotheses have been formulated in this framework, placing different emphasis on ecological, behavioural, or physiological aspects of trade-offs in brain size evolution. Within this body of work, there exists considerable taxonomic bias towards studies of birds and mammals, leaving some uncertainty about the generality of the respective arguments. Here, we test three of the most prominent such hypotheses, the ´expensive tissue´, ´social brain´, and ´cognitive buffer´ hypotheses, in a large dataset of fishes, derived from a publicly available resource (FishBase). In accordance with predictions from the ´expensive tissue´ and the ´social brain´ hypothesis, larger brains co-occur with reduced fecundity and increased sociality in at least some Classes of fish. Contrary to expectations, however, lifespan is reduced in large-brained fishes, and there is a tendency for species that perform parental care to have smaller brains. As such, it appears that some potential costs (reduced fecundity) and benefits (increased sociality) of large brains are near universal to vertebrates, while others have more lineage-specific effects. We discuss our findings in the context of fundamental differences between the classically studied birds and mammals and the fishes we analyse here, namely divergent patterns of growth, parenting, and neurogenesis. As such, our work highlights the need for a taxonomically diverse approach to any fundamental question in evolutionary biology.

This dataset includes all data used in the respective manuscript.

Using the R package rfishbase (version 3.1.6; (Boettiger et al. 2021)), we downloaded information from FishBase (www.fishbase.se; (Froese and Pauly 2000)) using the package’s default commands and functions (all data initially downloaded during the second half of March 2021). FishBase is a publicly available database and analysis tool with the aim ‘to provide key information on fishes of the world, that is both global and deep’ (Froese and Pauly 2000). For more than three decades, FishBase has pursued this goal by extracting data from the primary and secondary literature on fishes and collating it in a searchable digital repository. As such, a lot of information has been manually transcribed from scientific articles, books, and other forms of publishing into FishBase’s data structure, with the respective source being referenced in FishBase. It should thus be noted that the data found on FishBase is imperfect, either because existing information has not (yet) been included, information was included inaccurately (e.g. typos), or the information in the source material was already wrong (Froese and Pauly 2000). There are ongoing efforts to make FishBase as error-free as possible, and by being an openly available database in which only already published information is included, at least two lines of checks exist: first, data need to pass reviewing processes during their initial publication. Second, once data enter FishBase, they are subject to the scrutiny of its users, which has repeatedly led to updates and corrections (Froese and Pauly 2000). FishBase is thus the most reliable and comprehensive source of information for the greatest number of fish species currently available (Froese and Pauly 2000). Our aim here was to collate a comprehensive dataset of brain sizes and corresponding variables of interest that relate to our questions about (i) associations between brain size and certain life history parameters, (ii) co-evolutionary links between breeding systems and brain size, (iii) and potential influences of habitat features on brain size evolution. To this end, we pre-screened all data available on FishBase for relevant information and selected those variables that we deemed most biologically meaningful. We did not trace entries on FishBase back to their sources. We selected two life history parameters (longevity and fecundity), two aspects of breeding systems (mating system and post-zygotic parental care), and two habitat features (a pelagic or demersal lifestyle and the presence or absence of migrations between marine and freshwater habitats) for our analyses. Specifically, we first extracted data for each species from FishBase’s ‘Species Table’ using the rfishbase function ‘species’ (see (Froese and Pauly 2000) for descriptions of each of the FishBase-specific terms indicated by quotation marks). For each species, we included the scientific name (column name in the table: ‘Species’), habitat information (‘DemersPelag’ (indicating whether the species follows a demersal or pelagic lifestyle), ‘AnaCat’ (indicating whether the species migrates between marine and freshwater habitats or not)), life history information (‘LongevityWild, ‘LongevityCaptive’ (indicating lifespan estimates in years in the wild or in captivity, respectively)), and body size information (‘Length’ (length measurements in centimetres), ‘LengthTypeMaxM’ (indicating the type of length measurement provided; see Appendix S1), ‘Weight’ (weight measurements in grams)). This yielded a total of 34299 species entries. As FishBase’s ‘Orders Table’ is currently not available via rfishbase, we manually added information on higher taxonomic classifications from FishBase’s ‘Classification List’ (https://www.fishbase.se/tools/Classification/ClassificationList.php), yielding an entry for Genus, Family, Order, and Class for each of the 34299 species. Every species was classified as pelagic or demersal, and 4025 were classified as migratory between marine and freshwater habitats or as non-migratory. For 117 species, longevity data in years from both captivity and the wild was available, while at least one of these estimates was provided for 212 (captive) and 1341 (wild) species, respectively. We elected to use the larger of these two measurements wherever both were provided. A length measurement in centimetres was given for 30373 species, including information on the type of measuring procedure (e.g. standard length or fork length) in 30180 cases (see Appendix S1). Weight data in grams could be retrieved for 2184 species. Both length and weight data were provided as maximum values recorded for a given species. We then downloaded fecundity data using the rfishbase function ‘fecundity’ and including the columns ‘Species’, ‘FecundityMin’ (2300 entries for 1374 species), ‘FecundityMax’ (2607 entries for 1570 species), and ‘FecundityMean’ (112 entries for 88 species), where fecundity is given as the number of eggs/oocytes found in a single ripe female. We elected to use the maximum value provided in any of the fecundity data for each species, resulting in a total sample size of 1763 species. We downloaded information on the breeding system of each species using the rfishbase function ‘reproduction’ and including ‘Species’, ‘MatingSystem’ (995 species), ‘RepGuild1’ (10645 species), ‘RepGuild2’ (8218 species), and ‘ParentalCare’ (6761 species). We classified species as either monogamous or polygamous (pooling all species classified as polyandrous or promiscuous), and as either showing post-zygotic parental care (pooling all species that do not just scatter their eggs upon mating, see (Froese and Pauly 2000) for detailed descriptions of categories) or not performing care. This yielded a total of 995 species for which we had mating system information and 10655 species with information on post-zygotic parental care (also referred to as ‘parental care’ throughout the manuscript). Subsequently, we used the rfishbase function ‘brains’ to download a total of 5744 brain weights (‘BrainWeight’ in milligrams) and the weight of the corresponding donor individual (‘BodyWeight’ in grams) from FishBase, representing 1436 species (as above, we included ‘Species’ for later merging of information). Information on a donor individual’s sex was only available for 36 species and we thus omitted ‘Sex’ in our analyses. For each species for which multiple brain and donor weights were available, we chose to include in our species-comparisons only the data of the heaviest individual measured, making it more comparable to our other phenotypic information (maximum length, weight, lifespan, and fecundity). Notably, relative brain weight (brain weight divided by donor weight, referred to as ‘EncCoeff’ in FishBase) declines with body weight (and body length) both within and across species ((Kotrschal et al. 1998); Appendix S2). By considering only the data of the largest individual available, we minimise potential biases stemming from greater proportions of juveniles measured for some species.

ReadMe file for the article ‘The costs and benefits of larger brains in fishes’ in the Journal of Evolutionary Biology (JEB-2022-00020).

Files:

FischerJungwirth2022_JEB_S7_all.csv: includes information on 34299 species of fish

FischerJungwirth2022_JEB_S7_indbrains.csv: includes information of individual brain donor individuals

FischerJungwirth2022_JEB_S7_8speciesindbrains.csv: includes information of individual brain donor weights for 8 selected species with the largest sample size for a given Class

FischerJungwirth2022_JEB_S7_Publicationdata.csv: includes information on publications on brain size

FischerJungwirth2022_JEB_S8.R: R script to reproduce all analyses and figures

Columns in all:

SpecCode: FishBase’s unique code for each species

Species: the species’ full scientific name

Genus: the genus to which the species is assigned on FishBase

Family: the family to which the species is assigned on FishBase

Order: the order to which the species is assigned on FishBase

Class: the Class to which the species is assigned on FishBase

FamCode: FishBase’s unique code for each family

Subfamily: the name of a given subfamily as assigned to the species on FishBase

Marine: binary variable for whether the species is considered marine (1) or inhabits freshwater (0)

Pelagic: binary variable for whether the species is considered pelagic (1) or demersal (0)

Migratory: binary variable for whether the species is considered migratory (1) or not (0)

Social: binary variable for whether the species is considered social (1) or solitary (0)

Longevity: a single estimate of the species’ maximum lifespan in years

logLongevity: ln transformed values of Longevity

Length: a single estimate of the species’ maximum length in cm

logLength: ln transformed values of Length

LengthType: the type of measurement to derive the species’ maximum length (SL: standard length; TL: total length; FL: fork length; WD: disk width; NA: not specified)

Weight: a single estimate of the species’ maximum weight in g derived from all available data

logWeight: ln transformed values of Weight

MaxWeightSpecies: a single estimate of the species’ maximum weight in g derived from FishBase’s species table

MaxWeightIndWithBrain: the body weight in g of the heaviest brain donor individual for a given species

BrainWeightMaxWeightIndWithBrain: the brain weight in mg of the heaviest brain donor individual for a given species

logBrain: ln transformed values of BrainWeightMaxWeightIndWithBrain

RelBrainSize: the weight of the brain of the heaviest individual per species for which a brain weight was available divided by that individual's weight

MaxFecundity: the maximum number of eggs/oocytes recorded for the species

logFecundity: ln transformed values of MaxFecundity

MaxLarvalSize: the maximum size in mm at hatching or first feeding of the larvae for the species

DevTime: the minimum time in days it takes the species from egg laying to hatching

EggSize: the species' maximum recorded egg size in mm diameter

logEggSize: ln transformed values of EggSize

Monogamy: binary variable for whether the species is considered monogamous (1) or polygamous/promiscuous (0)

ParentalCare: binary variable for whether the species is performs some post-zygotic parental care (1) or only scatters its eggs (0)

Columns in indbrains:

SpecCode: FishBase’s unique code for each species

Species: the species’ full scientific name

Genus: the genus to which the species is assigned on FishBase

Family: the family to which the species is assigned on FishBase

Order: the order to which the species is assigned on FishBase

Class: the Class to which the species is assigned on FishBase

BodyWeight: the donor individual’s body weight in g

BrainWeight: the donor individual’s brain weight in mg

CountEntries: cumulative count of the number of brain weights recorded for the species (0 = no brain weight measurements available)

Columns in 8speciesindbrains:

SpecCode: FishBase’s unique code for each species

Species: the species’ full scientific name

Genus: the genus to which the species is assigned on FishBase

Family: the family to which the species is assigned on FishBase

Order: the order to which the species is assigned on FishBase

Class: the Class to which the species is assigned on FishBase

BodyWeight: the donor individual’s body weight in g

BrainWeight: the donor individual’s brain weight in mg

SL: the donor individual’s standard length in cm

TL: the donor individual’s total length in cm

SampleSize: the number of brain weights recorded for the species

Publicationdata:

Year: the year in which at least one paper on brain size was published

Nr publ: count of publications for a given taxon for a given year

Cum.Nr.publ: cumulative count of publications for a given taxon

Taxon: taxonomic group for which the publications were found (mammal, bird, or fish)