The influence of domestication, insularity and sociality on the tempo and mode of brain size evolution in mammals

Abstract The ability to develop complex social bonds and an increased capacity for behavioural flexibility in novel environments have both been forwarded as selective forces favouring the evolution of a large brain in mammals. However, large brains are energetically expensive, and in circumstances in which selective pressures are relaxed, e.g. on islands, smaller brains are selected for. Similar reasoning has been offered to explain the reduction of brain size in domestic species relative to their wild relatives. Herein, we assess the effect of domestication, insularity and sociality on brain size evolution at the macroevolutionary scale. Our results are based on analyses of a 426-taxon tree, including both wild species and domestic breeds. We further develop the phylogenetic ridge regression comparative method (RRphylo) to work with discrete variables and compare the rates (tempo) and direction (mode) of brain size evolution among categories within each of three factors (sociality, insularity and domestication). The common assertion that domestication increases the rate of brain size evolution holds true. The same does not apply to insularity. We also find support for the suggested but previously untested hypothesis that species living in medium-sized groups exhibit faster rates of brain size evolution than either solitary or herding taxa.

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Brain size evolution in small mammals: test of the expensive tissue hypothesis

Mammalia ◽

10.1515/mammalia-2019-0134 ◽

2021 ◽

Vol 0 (0) ◽

Author(s):

Ying Jiang ◽

Jia Yu Wang ◽

Xiao Fu Huang ◽

Chun Lan Mai ◽

Wen Bo Liao

Keyword(s):

Small Mammals ◽

Brain Size ◽

Reproductive Investment ◽

Generalized Least Squares ◽

Offspring Number ◽

Size Evolution ◽

Large Brain ◽

Species Evolution ◽

The Cost ◽

Expensive Tissue Hypothesis

Abstract Brain size exhibits significant changes within and between species. Evolution of large brains can be explained by the need to improve cognitive ability for processing more information in changing environments. However, brains are among the most energetically expensive organs. Enlarged brains can impose energetic demands that limit brain size evolution. The expensive tissue hypothesis (ETH) states that a decrease in the size of another expensive tissue, such as the gut, should compensate for the cost of a large brain. We studied the interplay between energetic limitations and brain size evolution in small mammals using phylogenetically generalized least squares (PGLS) regression analysis. Brain mass was not correlated with the length of the digestive tract in 37 species of small mammals after correcting for phylogenetic relationships and body size effects. We further found that the evolution of a large brain was not accompanied by a decrease in male reproductive investments into testes mass and in female reproductive investment into offspring number. The evolution of brain size in small mammals is inconsistent with the prediction of the ETH.

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Pattern and process in hominin brain size evolution are scale-dependent

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2017.2738 ◽

2018 ◽

Vol 285 (1873) ◽

pp. 20172738 ◽

Cited By ~ 23

Author(s):

Andrew Du ◽

Andrew M. Zipkin ◽

Kevin G. Hatala ◽

Elizabeth Renner ◽

Jennifer L. Baker ◽

...

Keyword(s):

Fossil Record ◽

Brain Size ◽

Exponential Model ◽

Human Fossil ◽

Hominin Evolution ◽

Size Evolution ◽

Large Brain ◽

Quantitative Basis ◽

Endocranial Volume ◽

Subsequent Disappearance

A large brain is a defining feature of modern humans, yet there is no consensus regarding the patterns, rates and processes involved in hominin brain size evolution. We use a reliable proxy for brain size in fossils, endocranial volume (ECV), to better understand how brain size evolved at both clade- and lineage-level scales. For the hominin clade overall, the dominant signal is consistent with a gradual increase in brain size. This gradual trend appears to have been generated primarily by processes operating within hypothesized lineages—64% or 88% depending on whether one uses a more or less speciose taxonomy, respectively. These processes were supplemented by the appearance in the fossil record of larger-brained Homo species and the subsequent disappearance of smaller-brained Australopithecus and Paranthropus taxa. When the estimated rate of within-lineage ECV increase is compared to an exponential model that operationalizes generation-scale evolutionary processes, it suggests that the observed data were the result of episodes of directional selection interspersed with periods of stasis and/or drift; all of this occurs on too fine a timescale to be resolved by the current human fossil record, thus producing apparent gradual trends within lineages. Our findings provide a quantitative basis for developing and testing scale-explicit hypotheses about the factors that led brain size to increase during hominin evolution.

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Island Rule, quantitative genetics and brain–body size evolution in Homo floresiensis

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2017.1065 ◽

2017 ◽

Vol 284 (1857) ◽

pp. 20171065 ◽

Cited By ~ 14

Author(s):

José Alexandre Felizola Diniz-Filho ◽

Pasquale Raia

Keyword(s):

Body Size ◽

Brain Size ◽

Natural Populations ◽

Direct Analysis ◽

Neutral Evolution ◽

Island Rule ◽

Selection Gradients ◽

Size Evolution ◽

Evolutionary Trajectories ◽

Selective Forces

Colonization of islands often activate a complex chain of adaptive events that, over a relatively short evolutionary time, may drive strong shifts in body size, a pattern known as the Island Rule. It is arguably difficult to perform a direct analysis of the natural selection forces behind such a change in body size. Here, we used quantitative evolutionary genetic models, coupled with simulations and pattern-oriented modelling, to analyse the evolution of brain and body size in Homo floresiensis , a diminutive hominin species that appeared around 700 kya and survived up to relatively recent times (60–90 kya) on Flores Island, Indonesia. The hypothesis of neutral evolution was rejected in 97% of the simulations, and estimated selection gradients are within the range found in living natural populations. We showed that insularity may have triggered slightly different evolutionary trajectories for body and brain size, which means explaining the exceedingly small cranial volume of H. floresiensis requires additional selective forces acting on brain size alone. Our analyses also support previous conclusions that H. floresiensis may be most likely derived from an early Indonesian H. erectus , which is coherent with currently accepted biogeographical scenario for Homo expansion out of Africa.

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Metabolic costs of brain size evolution

Biology Letters ◽

10.1098/rsbl.2006.0538 ◽

2006 ◽

Vol 2 (4) ◽

pp. 557-560 ◽

Cited By ~ 188

Author(s):

Karin Isler ◽

Carel P van Schaik

Keyword(s):

Brain Size ◽

Size Variation ◽

Brain Evolution ◽

Energy Costs ◽

Main Interest ◽

Ecological Benefits ◽

Size Evolution ◽

Large Brain ◽

Metabolic Costs ◽

Cognitive Benefits

Abstract In the ongoing discussion about brain evolution in vertebrates, the main interest has shifted from theories focusing on energy balance to theories proposing social or ecological benefits of enhanced intellect. With the availability of a wealth of new data on basal metabolic rate (BMR) and brain size and with the aid of reliable techniques of comparative analysis, we are able to show that in fact energetics is an issue in the maintenance of a relatively large brain, and that brain size is positively correlated with the BMR in mammals, controlling for body size effects. We conclude that attempts to explain brain size variation in different taxa must consider the ability to sustain the energy costs alongside cognitive benefits.

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Dolphin social intelligence: complex alliance relationships in bottlenose dolphins and a consideration of selective environments for extreme brain size evolution in mammals

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2006.1997 ◽

2007 ◽

Vol 362 (1480) ◽

pp. 587-602 ◽

Cited By ~ 135

Author(s):

Richard C Connor

Keyword(s):

Cognitive Abilities ◽

Social Intelligence ◽

Brain Size ◽

Bottlenose Dolphins ◽

Sperm Whale ◽

Shark Bay ◽

External Threats ◽

Size Evolution ◽

Large Brain ◽

Selection For

Bottlenose dolphins in Shark Bay, Australia, live in a large, unbounded society with a fission–fusion grouping pattern. Potential cognitive demands include the need to develop social strategies involving the recognition of a large number of individuals and their relationships with others. Patterns of alliance affiliation among males may be more complex than are currently known for any non-human, with individuals participating in 2–3 levels of shifting alliances. Males mediate alliance relationships with gentle contact behaviours such as petting, but synchrony also plays an important role in affiliative interactions. In general, selection for social intelligence in the context of shifting alliances will depend on the extent to which there are strategic options and risk. Extreme brain size evolution may have occurred more than once in the toothed whales, reaching peaks in the dolphin family and the sperm whale. All three ‘peaks’ of large brain size evolution in mammals (odontocetes, humans and elephants) shared a common selective environment: extreme mutual dependence based on external threats from predators or conspecific groups. In this context, social competition, and consequently selection for greater cognitive abilities and large brain size, was intense.

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No evidence for the expensive-tissue hypothesis in Fejervarya limnocharis

Animal Biology ◽

10.1163/15707563-17000094 ◽

2018 ◽

Vol 68 (3) ◽

pp. 265-276 ◽

Cited By ~ 3

Author(s):

Sheng Nan Yang ◽

Hao Feng ◽

Long Jin ◽

Zhao Min Zhou ◽

Wen Bo Liao

Keyword(s):

Brain Size ◽

Relative Size ◽

Trade Offs ◽

Size Evolution ◽

Large Brain ◽

Relative Brain Size ◽

The Cost ◽

Kidney Liver ◽

Expensive Tissue Hypothesis ◽

Fejervarya Limnocharis

AbstractBecause the brain is one of the energetically most expensive organs of animals, trade-offs have been hypothesized to exert constraints on brain size evolution. The expensive-tissue hypothesis predicts that the cost of a large brain should be compensated by decreasing size of other metabolically costly tissues, such as the gut. Here, we analyzed the relationships between relative brain size and the size of other metabolically costly tissues (i.e., gut, heart, lung, kidney, liver, spleen or limb muscles) among four Fejervarya limnocharis populations to test the predictions of the expensive-tissue hypothesis. We did not find that relative brain size was negatively correlated with relative gut length after controlling for body size, which was inconsistent with the prediction of the expensive-tissue hypothesis. We also did not find negative correlations between relative brain mass and relative size of the other energetically expensive organs. Our findings suggest that the cost of large brains in F. limnocharis cannot be compensated by decreasing size in other metabolically costly tissues.

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Different environmental variables predict body and brain size evolution in Homo

Nature Communications ◽

10.1038/s41467-021-24290-7 ◽

2021 ◽

Vol 12 (1) ◽

Author(s):

Manuel Will ◽

Mario Krapp ◽

Jay T. Stock ◽

Andrea Manica

Keyword(s):

Environmental Factors ◽

Cognitive Abilities ◽

Net Primary Productivity ◽

Brain Size ◽

Environmental Influence ◽

Size Variation ◽

Evolutionary Pattern ◽

Statistical Framework ◽

Size Evolution ◽

Major Predictor

AbstractIncreasing body and brain size constitutes a key macro-evolutionary pattern in the hominin lineage, yet the mechanisms behind these changes remain debated. Hypothesized drivers include environmental, demographic, social, dietary, and technological factors. Here we test the influence of environmental factors on the evolution of body and brain size in the genus Homo over the last one million years using a large fossil dataset combined with global paleoclimatic reconstructions and formalized hypotheses tested in a quantitative statistical framework. We identify temperature as a major predictor of body size variation within Homo, in accordance with Bergmann’s rule. In contrast, net primary productivity of environments and long-term variability in precipitation correlate with brain size but explain low amounts of the observed variation. These associations are likely due to an indirect environmental influence on cognitive abilities and extinction probabilities. Most environmental factors that we test do not correspond with body and brain size evolution, pointing towards complex scenarios which underlie the evolution of key biological characteristics in later Homo.

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Mind the Gap: Why the Landscape Planning System in Sardinia Does Not Work

Sustainability ◽

10.3390/su13137300 ◽

2021 ◽

Vol 13 (13) ◽

pp. 7300

Author(s):

Anna Maria Colavitti ◽

Alessio Floris ◽

Sergio Serra

Keyword(s):

Landscape Planning ◽

Comparative Method ◽

Poor Quality ◽

Planning System ◽

Local Planning ◽

The Common ◽

Regional Landscape ◽

Landscape Protection

In Italy, after the introduction of the Code of Cultural Heritage and Landscape in 2004, the Regional Landscape Plan (RLP) has acquired a coordination role in the urban planning system, for the implementation of policies for landscape protection and valorisation. The case study of the RLP of Sardinia is a paradigmatic application to the coastal area of the island, which is considered most vulnerable and subject to settlement pressure. The objectives of preservation and valorisation of the territorial resources should be transferred into local planning instruments by adopting strategies aimed at the preservation of the consolidated urban fabric, at the requalification and completion of the existing built-up areas according to the principles of land take limitation and increase in urban quality. The paper investigates the state of implementation and the level of integration of landscape contents in the local plans that have been adapted to the RLP, using a qualitative comparative method. In addition, the results of the plan coherence checks, elaborated by the regional monitoring bodies after the adaptation process, have been analysed to identify the common criticalities and weaknesses. The results highlight the lack of effectiveness of the RLP, after more than a decade since its approval, considering the limited number of adequate local plans and the poor quality of their analytical and regulative contents in terms of landscape protection and valorisation. Conclusions suggest some possible ways to revise the RLP, focusing on the participation of local communities and the development of a new landscape culture.

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