Hippocampal (HC) volume has been hypothesized to increase with an increase in food-hoarding specialization in corvids and parids. Recent studies revealed that (i) the HC/hoarding relationship is significant when a difference in HC volume between Eurasian and North American species is controlled for and (ii) the evolutionary association has been acting on a broader phylogenetic context involving avian families outside the Corvidae and Paridae. However, the phylogenetic extent of the continent effect has not been previously addressed. Using data representing 48 avian species, we performed a phylogenetic analysis to test if continental effects are important in a wider evolutionary spectrum. Our results support the observation that Eurasian species have generally larger HC than North American species if variation in food hoarding, which also varied between continents, was held constant. Surprisingly, the relationship between continental distribution and relative HC volume was significant when we included only non-hoarding families in our analysis, indicating that the extent of the continent effect is much broader than originally described. We investigated the potential role of minimal winter temperatures at the northernmost distribution borders in mediating continent effects. The effect of winter temperatures on HC volume was weak and it did not vary consistently along continents. We suggest that the general continental differences in relative HC size are independent of food hoarding and that its determinants should be sought among other ecological factors and life-history traits.
doi:10.1098/rsbl.2005.0328
PMCID: PMC1523380
PMID: 16878181
Corvidae; food caching; hippocampus; Paridae; phylogeny
Paternal behaviour is critical for the survival of offspring in many monogamous species. Common marmoset (Callithrix jacchus) and cotton-top tamarin (Saguinus oedipus) fathers spend as much or more time caring for infants than mothers. Expectant males of both species showed significant increases in weight across the pregnancy whereas control males did not (five consecutive months for marmoset males and six months for cotton-top tamarin males). Expectant fathers might be preparing for the energetic cost of fatherhood by gaining weight during their mate’s pregnancy.
doi:10.1098/rsbl.2005.0426
PMCID: PMC1483903
PMID: 16810338
weight gain; paternal care; couvades; primates
Paternal behaviour is critical for the survival of offspring in many monogamous species. Common marmoset (Callithrix jacchus) and cotton-top tamarin (Saguinus oedipus) fathers spend as much or more time caring for infants than mothers. Expectant males of both species showed significant increases in weight across the pregnancy whereas control males did not (five consecutive months for marmoset males and six months for cotton-top tamarin males). Expectant fathers might be preparing for the energetic cost of fatherhood by gaining weight during their mate's pregnancy.
doi:10.1098/rsbl.2005.0426
PMCID: PMC1483903
PMID: 16810338
weight gain; paternal care; couvade; primates
Hippocampal (HC) volume has been hypothesized to increase with an increase in food-hoarding specialization in corvids and parids. Recent studies revealed that (i) the HC/hoarding relationship is significant when a difference in HC volume between Eurasian and North American species is controlled for and (ii) the evolutionary association has been acting on a broader phylogenetic context involving avian families outside the Corvidae and Paridae. However, the phylogenetic extent of the continent effect has not been previously addressed. Using data representing 48 avian species, we performed a phylogenetic analysis to test if continental effects are important in a wider evolutionary spectrum. Our results support the observation that Eurasian species have generally larger HC than North American species if variation in food hoarding, which also varied between continents, was held constant. Surprisingly, the relationship between continental distribution and relative HC volume was significant when we included only non-hoarding families in our analysis, indicating that the extent of the continent effect is much broader than originally described. We investigated the potential role of minimal winter temperatures at the northernmost distribution borders in mediating continent effects. The effect of winter temperatures on HC volume was weak and it did not vary consistently along continents. We suggest that the general continental differences in relative HC size are independent of food hoarding and that its determinants should be sought among other ecological factors and life-history traits.
doi:10.1098/rsbl.2005.0328
PMCID: PMC1523380
PMID: 16878181
Corvidae; food caching; hippocampus; Paridae; phylogeny
doi:10.1098/rsbl.2012.0777
PMCID: PMC3497148
PMID: 22940673
doi:10.1098/rsbl.2011.1225
PMCID: PMC3297410
doi:10.1098/rsbl.2011.0376
PMCID: PMC3259945
PMID: 21543393
Modelling has been underdeveloped with respect to constructing palaeobiodiversity curves, but it offers an additional tool for removing sampling from their estimation. Here, an alternative to subsampling approaches, which often require large sample sizes, is explored by the extension and refinement of a pre-existing modelling technique that uses a geological proxy for sampling. Application of the model to the three main clades of dinosaurs suggests that much of their diversity fluctuations cannot be explained by sampling alone. Furthermore, there is new support for a long-term decline in their diversity leading up to the Cretaceous–Paleogene (K–Pg) extinction event. At present, use of this method with data that includes either Lagerstätten or ‘Pull of the Recent’ biases is inappropriate, although partial solutions are offered.
doi:10.1098/rsbl.2011.0210
PMCID: PMC3259943
PMID: 21508029
modelling; sampling bias; palaeobiodiversity; subsampling; dinosaurs
Accumulations of dead skeletal material are a valuable archive of past ecological conditions. However, such assemblages are not equivalent to living communities because they mix the remains of multiple generations and are altered by post-mortem processes. The abundance of a species in a death assemblage can be quantitatively modelled by successively integrating the product of an influx time series and a post-mortem loss function (a decay function with a constant half-life). In such a model, temporal mixing increases expected absolute dead abundance relative to average influx as a linear function of half-life and increases variation in absolute dead abundance values as a square-root function of half-life. Because typical abundance distributions of ecological communities are logarithmically distributed, species' differences in preservational half-life would have to be very large to substantially alter species' abundance ranks (i.e. make rare species common or vice-versa). In addition, expected dead abundances increase at a faster rate than their range of variation with increased time averaging, predicting greater consistency in the relative abundance structure of death assemblages than their parent living community.
doi:10.1098/rsbl.2011.0337
PMCID: PMC3259944
PMID: 21653564
time averaging; death assemblage; fossil assemblage; convolution; moving average process
Biomechanical modelling and simulation techniques offer some hope for unravelling the complex inter-relationships of structure and function perhaps even for extinct organisms, but have their limitations owing to this complexity and the many unknown parameters for fossil taxa. Validation and sensitivity analysis are two indispensable approaches for quantifying the accuracy and reliability of such models or simulations. But there are other subtleties in biomechanical modelling that include investigator judgements about the level of simplicity versus complexity in model design or how uncertainty and subjectivity are dealt with. Furthermore, investigator attitudes toward models encompass a broad spectrum between extreme credulity and nihilism, influencing how modelling is conducted and perceived. Fundamentally, more data and more testing of methodology are required for the field to mature and build confidence in its inferences.
doi:10.1098/rsbl.2011.0399
PMCID: PMC3259946
PMID: 21666064
musculoskeletal system; dinosaur; computer modelling; simulation; palaeontology; biomechanics
In indigenous arctic reindeer and ptarmigan, circadian rhythms are not expressed during the constant light of summer or constant dark of winter, and it has been hypothesized that a seasonal absence of circadian rhythms is common to all vertebrate residents of polar regions. Here, we show that, while free-living arctic ground squirrels do not express circadian rhythms during the heterothermic and pre-emergent euthermic intervals of hibernation, they display entrained daily rhythms of body temperature (Tb) throughout their active season, which includes six weeks of constant sun. In winter, ground squirrels are arrhythmic and regulate core body temperatures to within ±0.2°C for up to 18 days during steady-state torpor. In spring, after the use of torpor ends, male but not female ground squirrels, resume euthermic levels of Tb in their dark burrows but remain arrhythmic for up to 27 days. However, once activity on the surface begins, both sexes exhibit robust 24 h cycles of body temperature. We suggest that persistence of nycthemeral rhythms through the polar summer enables ground squirrels to minimize thermoregulatory costs. However, the environmental cues (zeitgebers) used to entrain rhythms during the constant light of the arctic summer in these semi-fossorial rodents are unknown.
doi:10.1098/rsbl.2011.0435
PMCID: PMC3259947
PMID: 21752811
circadian rhythms; zeitgeber; body temperature; torpor; arctic ground squirrel
Statistical models are helping palaeontologists to elucidate the history of biodiversity. Sampling standardization has been extensively applied to remedy the effects of uneven sampling in large datasets of fossil invertebrates. However, many vertebrate datasets are smaller, and the issue of uneven sampling has commonly been ignored, or approached using pairwise comparisons with a numerical proxy for sampling effort. Although most authors find a strong correlation between palaeodiversity and sampling proxies, weak correlation is recorded in some datasets. This has led several authors to conclude that uneven sampling does not influence our view of vertebrate macroevolution. We demonstrate that multi-variate regression models incorporating a model of underlying biological diversification, as well as a sampling proxy, fit observed sauropodomorph dinosaur palaeodiversity best. This bivariate model is a better fit than separate univariate models, and illustrates that observed palaeodiversity is a composite pattern, representing a biological signal overprinted by variation in sampling effort. Multi-variate models and other approaches that consider sampling as an essential component of palaeodiversity are central to gaining a more complete understanding of deep time vertebrate diversification.
doi:10.1098/rsbl.2011.0460
PMCID: PMC3259948
PMID: 21697163
multi-variate models; palaeodiversity; sauropodomorpha
Despite much interest in amniote systematics, the origin of turtles remains elusive. Traditional morphological phylogenetic analyses place turtles outside Diapsida—amniotes whose ancestor had two fenestrae in the temporal region of the skull (among the living forms the tuatara, lizards, birds and crocodilians)—and allied with some unfenestrate-skulled (anapsid) taxa. Nonetheless, some morphological analyses place turtles within Diapsida, allied with Lepidosauria (tuatara and lizards). Most molecular studies agree that turtles are diapsids, but rather than allying them with lepidosaurs, instead place turtles near or within Archosauria (crocodilians and birds). Thus, three basic phylogenetic positions for turtles with respect to extant Diapsida are currently debated: (i) sister to Diapsida, (ii) sister to Lepidosauria, or (iii) sister to, or within, Archosauria. Interestingly, although these three alternatives are consistent with a single unrooted four-taxon tree for extant reptiles, they differ with respect to the position of the root. Here, we apply a novel molecular dataset, the presence versus absence of specific microRNAs, to the problem of the phylogenetic position of turtles and the root of the reptilian tree, and find that this dataset unambiguously supports a turtle + lepidosaur group. We find that turtles and lizards share four unique miRNA gene families that are not found in any other organisms' genome or small RNA library, and no miRNAs are found in all diapsids but not turtles, or in turtles and archosaurs but not in lizards. The concordance between our result and some morphological analyses suggests that there have been numerous morphological convergences and reversals in reptile phylogeny, including the loss of temporal fenestrae.
doi:10.1098/rsbl.2011.0477
PMCID: PMC3259949
PMID: 21775315
turtle; microRNA; amniote
The role of behavioural flexibility in responding to new or changing environmental challenges is a central theme in cognitive ecology. Studies of behavioural flexibility have focused mostly on mammals and birds because theory predicts that behavioural flexibility is favoured in species or clades that exploit a diversity of habitats or food sources and/or have complex social structure, attributes not associated with ectothermic vertebrates. Here, we present the results of a series of experiments designed to test cognitive abilities across multiple cognitive modules in a tropical arboreal lizard: Anolis evermanni. This lizard shows behavioural flexibility across multiple cognitive tasks, including solving a novel motor task using multiple strategies and reversal learning, as well as rapid associative learning. This flexibility was unexpected because lizards are commonly believed to have limited cognitive abilities and highly stereotyped behaviour. Our findings indicate that the cognitive abilities of A. evermanni are comparable with those of some endothermic species that are recognized to be highly flexible, and strongly suggest a re-thinking of our understanding of the cognitive abilities of ectothermic tetrapods and of the factors favouring the evolution of behavioural flexibility.
doi:10.1098/rsbl.2011.0480
PMCID: PMC3259950
PMID: 21752816
behavioural flexibility; cognition; evolution; reptile; radiation; Anolis
Talpid moles across all northern continents exhibit a remarkably large, sickle-like radial sesamoid bone anterior to their five digits, always coupled with a smaller tibial sesamoid bone. A possible developmental mechanism behind this phenomenon was revealed using molecular markers during limb development in the Iberian mole (Talpa occidentalis) and a shrew (Cryptotis parva), as shrews represent the closest relatives of moles but do not show these conspicuous elements. The mole's radial sesamoid develops later than true digits, as shown by Sox9, and extends into the digit area, developing in relation to an Msx2-domain at the anterior border of the digital plate. Fgf8 expression, marking the apical ectodermal ridge, is comparable in both species. Developmental peculiarities facilitated the inclusion of the mole's radial sesamoid into the digit series; talpid moles circumvent the almost universal pentadactyly constraint by recruiting wrist sesamoids into their digital region using a novel developmental pathway and timing.
doi:10.1098/rsbl.2011.0494
PMCID: PMC3259951
PMID: 21752813
Talpidae; os falciforme; autopodial development
The distribution of species among genera and higher taxa has largely untapped potential to reveal among-clade variation in rates of origination and extinction. The probability distribution of the number of species within a genus is modelled with a stochastic, time-homogeneous birth–death model having two parameters: the rate of species extinction, μ, and the rate of genus origination, γ, each scaled as a multiple of the rate of within-genus speciation, λ. The distribution is more sensitive to γ than to μ, although μ affects the size of the largest genera. The species : genus ratio depends strongly on both γ and μ, and so is not a good diagnostic of evolutionary dynamics. The proportion of monotypic genera, however, depends mainly on γ, and so may provide an index of the genus origination rate. Application to living marine molluscs of New Zealand shows that bivalves have a higher relative rate of genus origination than gastropods. This is supported by the analysis of palaeontological data. This concordance suggests that analysis of living taxonomic distributions may allow inference of macroevolutionary dynamics even without a fossil record.
doi:10.1098/rsbl.2011.0521
PMCID: PMC3259952
PMID: 21865239
evolutionary rates; hollow curve; mathematical modelling; New Zealand; Mollusca
Rate distributions are important considerations when testing hypotheses about morphological evolution or phylogeny. They also have implications about general processes underlying character evolution. Molecular systematists often assume that rates are Poisson processes with gamma distributions. However, morphological change is the product of multiple probabilistic processes and should theoretically be affected by hierarchical integration of characters. Both factors predict lognormal rate distributions. Here, a simple inverse modelling approach assesses the best single-rate, gamma and lognormal models given observed character compatibility for 115 invertebrate groups. Tests reject the single-rate model for nearly all cases. Moreover, the lognormal outperforms the gamma for character change rates and (especially) state derivation rates. The latter in particular is consistent with integration affecting morphological character evolution.
doi:10.1098/rsbl.2011.0523
PMCID: PMC3259953
PMID: 21795266
character evolution; compatibility; lognormal distribution; gamma distribution; information theory
Rhesus monkeys (Macaca mulatta) have shown the ability to monitor their own mental states, but fail the mirror self-recognition test. In humans, the sense of self-agency is closely related to self-awareness, and results from monitoring the relationship between intentional, sensorimotor and perceptual information. Humans and rhesus monkeys were trained to move a computer icon with a joystick while a distractor icon partially matched their movements. Both humans and monkeys were able to monitor and identify the icon they were controlling, suggesting they have some understanding of self-agency.
doi:10.1098/rsbl.2011.0536
PMCID: PMC3259954
PMID: 21733868
self-agency; self-awareness; rhesus monkeys
Males in many taxa are known to exhibit behavioural plasticity in response to the perceived intensity of sperm competition, reflected in Drosophila melanogaster by increased copulation duration following prior exposure to a rival. We tested the prediction that males do not adjust their copulation effort in response to the presence of a competitor in Drosophila species where there is little or no sperm competition. Contrary to expectations, male plasticity in copulation duration was found in both Drosophila subobscura and Drosophila acanthoptera, species in which females rarely remate. These results are discussed in relation to the adaptive basis of plasticity in these species.
doi:10.1098/rsbl.2011.0544
PMCID: PMC3259955
PMID: 21752815
plasticity; monandry; polyandry; copulation duration; female receptivity; social environment
Human and livestock diseases can be difficult to control where infection persists in wildlife populations. Control of bovine tuberculosis (bTB) in British cattle is complicated by the maintenance of Mycobacterium bovis (the causative agent of bTB) in badgers, acting as reservoirs of infection. Although over 20 000 badgers were culled to control bTB between 1975 and 1997, the incidence of bTB in cattle has substantially increased in parts of Great Britain in recent decades. Our case-control study, involving 1208 cattle herds, provides further evidence of the detrimental effect of localized reactive badger culling in response to the disclosure of a confirmed bTB herd breakdown in cattle. The presence of any reactive badger culling activity and increased numbers of badgers culled in the vicinity of a herd were associated with significantly increased bTB risk, even after adjusting for other important local risk factors. Such findings may partly explain why some earlier localized approaches to bTB control were ineffective.
doi:10.1098/rsbl.2011.0554
PMCID: PMC3259956
PMID: 21752812
bovine tuberculosis; case-control study; localized reactive badger culling; Randomized Badger Culling Trial
Allogrooming occurs in a wide range of species and can serve both hygienic and social functions. While the latter have long been thought to be underpinned by reductions in tension for recipients, recent work has suggested that donors may also benefit in this way. Here, I show that, in cooperatively breeding green woodhoopoes Phoeniculus purpureus, involvement in allogrooming is followed by a reduction in self-grooming by both recipients and donors, but that the former exhibit a greater decrease. Moreover, I demonstrate for the first time that the dominance status of the allogrooming participant is important, with subordinate group members reducing subsequent self-grooming to a greater extent than the dominant pair. If avian self-directed behaviour reflects current distress levels in the same way as found in various primates, my results would indicate that allogrooming benefits are not confined to mammals, and would have important implications both for accurate assessments of the true costs and benefits of affiliative behaviour and for our understanding of the evolution of sociality.
doi:10.1098/rsbl.2011.0559
PMCID: PMC3259957
PMID: 21795264
affiliation; cooperation; grooming; group-living; stress
Ambient light levels influence visual system size in birds and primates. Here, we argue that the same is true for humans. Light levels, in terms of both the amount of light hitting the Earth's surface and day length, decrease with increasing latitude. We demonstrate a significant positive relationship between absolute latitude and human orbital volume, an index of eyeball size. Owing to tight scaling between visual system components, this will translate into enlarged visual cortices at higher latitudes. We also show that visual acuity measured under full-daylight conditions is constant across latitudes, indicating that selection for larger visual systems has mitigated the effect of reduced ambient light levels. This provides, to our knowledge, the first support that light levels drive intraspecific variation in visual system size in the human population.
doi:10.1098/rsbl.2011.0570
PMCID: PMC3259958
PMID: 21795263
latitude; light levels; eyeball size; visual cortex size; day length
The distance that animals leap depends on their take-off angle and velocity. The velocity is generated solely by mechanical work during the push-off phase of standing-start leaps. Gibbons are capable of exceptional leaping performance, crossing gaps in the forest canopy exceeding 10 m, yet possess none of the adaptations possessed by specialist leapers synonymous with maximizing mechanical work. To understand this impressive performance, we recorded leaps of the gibbons exceeding 3.7 m. Gibbons perform more mass-specific work (35.4 J kg−1) than reported for any other species to date, accelerating to 8.3 ms−1 in a single movement and redefining our estimates of work performance by animals. This energy (enough for a 3.5 m vertical leap) is 60 per cent higher than that achieved by galagos, which are renowned for their remarkable leaping performance. The gibbons' unusual morphology facilitates a division of labour among the hind limbs, forelimbs and trunk, resulting in modest power requirements compared with more specialized leapers.
doi:10.1098/rsbl.2011.0574
PMCID: PMC3259959
PMID: 21831879
leaping; work; power; primate; gibbon
North Atlantic right whales are critically endangered and, despite international protection from whaling, significant numbers die from collisions with ships. Large groups of right whales migrate to the coastal waters of New England during the late winter and early spring to feed in an area with large numbers of vessels. North Atlantic right whales have the largest per capita record of vessel strikes of any large whale population in the world. Right whale feeding behaviour in Cape Cod Bay (CCB) probably contributes to risk of collisions with ships. In this study, feeding right whales tagged with archival suction cup tags spent the majority of their time just below the water's surface where they cannot be seen but are shallow enough to be vulnerable to ship strike. Habitat surveys show that large patches of right whale prey are common in the upper 5 m of the water column in CCB during spring. These results indicate that the typical spring-time foraging ecology of right whales may contribute to their high level of mortality from vessel collisions. The results of this study suggest that remote acoustic detection of prey aggregations may be a useful supplement to the management and conservation of right whales.
doi:10.1098/rsbl.2011.0578
PMCID: PMC3259960
PMID: 21813549
foraging ecology; endangered species; vessel collision; right whale
The four-eyed fish, Anableps anableps, has eyes with unusual morphological adaptations for simultaneous vision above and below water. The retina, for example, is divided such that one region receives light from the aerial field and the other from the aquatic field. To understand better the adaptive value of this partitioned retina, we characterized photoreceptor distribution using in situ hybridization. Cones expressing sws1, sws2b and rh2-2 (i.e. UV, and short wavelength-sensitive) opsins were found throughout the retina, whereas cones expressing rh2-1 (middle wavelength-sensitive) were largely limited to the ventral retina and those expressing lws (long wavelength-sensitive) opsins were only expressed in the dorsal retina. We next asked when this pattern evolved relative to the ‘four-eyed’ morphology. We characterized opsin expression in Jenynsia onca, a member of the sister genus to Anableps with typical teleost eye morphology. In J. onca, sws1, sws2b, rh2-2 and rh2-1 opsins were expressed throughout the retina; while lws opsins were not expressed in the ventral retina. Thus, the change that coincides with the evolution of unusual anablepid eye morphology is the loss of rh2-1 expression in the dorsal retina, probably to accommodate increased lws opsin expression. The retinal area that samples aerial light appears not to have changed with respect to photoreceptor transcription.
doi:10.1098/rsbl.2011.0582
PMCID: PMC3259961
PMID: 21775314
fish; visual pigment; wavelength sensitivity; intraretinal variability; spectral tuning; retinal topography