Mode and tempo in the evolution of socio-political organization: reconciling 'Darwinian' and 'Spencerian' evolutionary approaches in anthropology

Traditional investigations of the evolution of human social and political institutions trace their ancestry back to nineteenth century social scientists such as Herbert Spencer, and have concentrated on the increase in socio-political complexity over time. More recent studies of cultural evolution have been explicitly informed by Darwinian evolutionary theory and focus on the transmission of cultural traits between individuals. These two approaches to investigating cultural change are often seen as incompatible. However, we argue that many of the defining features and assumptions of 'Spencerian' cultural evolutionary theory represent testable hypotheses that can and should be tackled within a broader 'Darwinian' framework. In this paper we apply phylogenetic comparative techniques to data from Austronesian-speaking societies of Island South-East Asia and the Pacific to test hypotheses about the mode and tempo of human socio-political evolution. We find support for three ideas often associated with Spencerian cultural evolutionary theory: (i) political organization has evolved through a regular sequence of forms, (ii) increases in hierarchical political complexity have been more common than decreases, and (iii) political organization has co-evolved with the wider presence of hereditary social stratification.     

Your place or mine? A phylogenetic comparative analysis of marital residence in Indo-European and Austronesian societies

Accurate reconstruction of prehistoric social organization is important if we are to put together satisfactory multidisciplinary scenarios about, for example, the dispersal of human groups. Such considerations apply in the case of Indo-European and Austronesian, two large-scale language families that are thought to represent Neolithic expansions. Ancestral kinship patterns have mostly been inferred through reconstruction of kin terminologies in ancestral proto-languages using the linguistic comparative method, and through geographical or distributional arguments based on the comparative patterns of kin terms and ethnographic kinship 'facts'. While these approaches are detailed and valuable, the processes through which conclusions have been drawn from the data fail to provide explicit criteria for systematic testing of alternative hypotheses. Here, we use language trees derived using phylogenetic tree-building techniques on Indo-European and Austronesian vocabulary data. With these trees, ethnographic data and Bayesian phylogenetic comparative methods, we statistically reconstruct past marital residence and infer rates of cultural change between different residence forms, showing Proto-Indo-European to be virilocal and Proto-Malayo-Polynesian uxorilocal. The instability of uxorilocality and the rare loss of virilocality once gained emerge as common features of both families.     

Evolution of breeding plumages in birds: A multiple‐step pathway to seasonal dichromatism in New World warblers (Aves: Parulidae)

Many species of birds show distinctive seasonal breeding and nonbreeding plumages. A number of hypotheses have been proposed for the evolution of this seasonal dichromatism, specifically related to the idea that birds may experience variable levels of sexual selection relative to natural selection throughout the year. However, these hypotheses have not addressed the selective forces that have shaped molt, the underlying mechanism of plumage change. Here, we examined relationships between life‐history variation, the evolution of a seasonal molt, and seasonal plumage dichromatism in the New World warblers (Aves: Parulidae), a family with a remarkable diversity of plumage, molt, and life‐history strategies. We used phylogenetic comparative methods and path analysis to understand how and why distinctive breeding and nonbreeding plumages evolve in this family. We found that color change alone poorly explains the evolution of patterns of biannual molt evolution in warblers. Instead, molt evolution is better explained by a combination of other life‐history factors, especially migration distance and foraging stratum. We found that the evolution of biannual molt and seasonal dichromatism is decoupled, with a biannual molt appearing earlier on the tree, more dispersed across taxa and body regions, and correlating with separate life‐history factors than seasonal dichromatism. This result helps explain the apparent paradox of birds that molt biannually but show breeding plumages that are identical to the nonbreeding plumage. We find support for a two‐step process for the evolution of distinctive breeding and nonbreeding plumages: That prealternate molt evolves primarily under selection for feather renewal, with seasonal color change sometimes following later. These results reveal how life‐history strategies and a birds' environment act upon multiple and separate feather functions to drive the evolution of feather replacement patterns and bird coloration.     

Is horizontal transmission really a problem for phylogenetic comparative methods? A simulation study using continuous cultural traits

Phylogenetic comparative methods (PCMs) provide a potentially powerful toolkit for testing hypotheses about cultural evolution. Here, we build on previous simulation work to assess the effect horizontal transmission between cultures has on the ability of both phylogenetic and non-phylogenetic methods to make inferences about trait evolution. We found that the mode of horizontal transmission of traits has important consequences for both methods. Where traits were horizontally transmitted separately, PCMs accurately reported when trait evolution was not correlated even at the highest levels of horizontal transmission. By contrast, linear regression analyses often incorrectly concluded that traits were correlated. Where simulated trait evolution was not correlated and traits were horizontally transmitted as a pair, both methods inferred increased levels of positive correlation with increasing horizontal transmission. Where simulated trait evolution was correlated, increasing rates of separate horizontal transmission led to decreasing levels of inferred correlation for both methods, but increasing rates of paired horizontal transmission did not. Furthermore, the PCM was also able to make accurate inferences about the ancestral state of traits. These results suggest that under certain conditions, PCMs can be robust to the effects of horizontal transmission. We discuss ways that future work can investigate the mode and tempo of horizontal transmission of cultural traits.     

A new phylogenetic test for comparing multiple high‐dimensional evolutionary rates suggests interplay of evolutionary rates and modularity in lanternfishes (Myctophiformes; Myctophidae)

The interplay between evolutionary rates and modularity influences the evolution of organismal body plans by both promoting and constraining the magnitude and direction of trait response to ecological conditions. However, few studies have examined whether the best‐fit hypothesis of modularity is the same as the shape subset with the greatest difference in evolutionary rate. Here, we develop a new phylogenetic comparative method for comparing evolutionary rates among high‐dimensional traits, and apply this method to analyze body shape evolution in bioluminescent lanternfishes. We frame the study of evolutionary rates and modularity through analysis of three hypotheses derived from the literature on fish development, biomechanics, and bioluminescent communication. We show that a development‐informed partitioning of shape exhibits the greatest evolutionary rate differences among modules, but that a hydrodynamically informed partitioning is the best‐fit modularity hypothesis. Furthermore, we show that bioluminescent lateral photophores evolve at a similar rate as, and are strongly integrated with, body shape in lanternfishes. These results suggest that overlapping life‐history constraints on development and movement define axes of body shape evolution in lanternfishes, and that the positions of their lateral photophore complexes are likely a passive outcome of the interaction of these ecological pressures.     

Cultural phylogeography of the Bantu Languages of sub-Saharan Africa

There is disagreement about the routes taken by populations speaking Bantu languages as they expanded to cover much of sub-Saharan Africa. Here, we build phylogenetic trees of Bantu languages and map them onto geographical space in order to assess the likely pathway of expansion and test between dispersal scenarios. The results clearly support a scenario in which groups first moved south through the rainforest from a homeland somewhere near the Nigeria–Cameroon border. Emerging on the south side of the rainforest, one branch moved south and west. Another branch moved towards the Great Lakes, eventually giving rise to the monophyletic clade of East Bantu languages that inhabit East and Southeastern Africa. These phylogenies also reveal information about more general processes involved in the diversification of human populations into distinct ethnolinguistic groups. Our study reveals that Bantu languages show a latitudinal gradient in covering greater areas with increasing distance from the equator. Analyses suggest that this pattern reflects a true ecological relationship rather than merely being an artefact of shared history. The study shows how a phylogeographic approach can address questions relating to the specific histories of certain groups, as well as general cultural evolutionary processes.     

Identifying innovation in laboratory studies of cultural evolution: rates of retention and measures of adaptation

In recent years, laboratory studies of cultural evolution have become increasingly prevalent as a means of identifying and understanding the effects of cultural transmission on the form and functionality of transmitted material. The datasets generated by these studies may provide insights into the conditions encouraging, or inhibiting, high rates of innovation, as well as the effect that this has on measures of adaptive cultural change. Here we review recent experimental studies of cultural evolution with a view to elucidating the role of innovation in generating observed trends. We first consider how tasks are presented to participants, and how the corresponding conceptualization of task success is likely to influence the degree of intent underlying any deviations from perfect reproduction. We then consider the measures of interest used by the researchers to track the changes that occur as a result of transmission, and how these are likely to be affected by differing rates of retention. We conclude that considering studies of cultural evolution from the perspective of innovation provides us with valuable insights that help to clarify important differences in research designs, which have implications for the likely effects of variation in retention rates on measures of cultural adaptation.     

Evolution of the genomic rate of recombination in mammals

Rates of recombination vary considerably between species. Despite the significance of this observation for evolutionary biology and genetics, the evolutionary mechanisms that contribute to these interspecific differences are unclear. On fine physical scales, recombination rates appear to evolve rapidly between closely related species, but the mode and tempo of recombination rate evolution on the broader scale is poorly understood. Here, we use phylogenetic comparative methods to begin to characterize the evolutionary processes underlying average genomic recombination rates in mammals. We document a strong phylogenetic effect in recombination rates, indicating that more closely related species tend to have more similar average rates of recombination. We demonstrate that this phylogenetic signal is not an artifact of errors in recombination rate estimation and show that it is robust to uncertainty in the mammalian phylogeny. Neutral evolutionary models present good fits to the data and we find no evidence for heterogeneity in the rate of evolution in recombination across the mammalian tree. These results suggest that observed interspecific variation in average genomic rates of recombination is largely attributable to the steady accumulation of neutral mutations over evolutionary time. Although single recombination hotspots may live and die on short evolutionary time scales, the strong phylogenetic signal in genomic recombination rates indicates that the pace of evolution on this scale may be considerably slower.     

Dietary adaptations in the teeth of murine rodents (Muridae): a test of biomechanical predictions

Functional dental theory predicts that tooth shape responds evolutionarily to the mechanical properties of food. Most studies of mammalian teeth have focused on qualitative measures of dental anatomy and have not formally tested how the functional components of teeth adapt in response to diet. Here we generated a series of predictions for tooth morphology based on biomechanical models of food processing. We used murine rodents (Old World rats and mice) to test these predictions for the relationship between diet and morphology and to identify a suite of functional dental characteristics that best predict diets. One hundred and five dental characteristics were extracted from images of the upper and lower tooth rows and incisors for 98 species. After accounting for phylogenetic relationships, we showed that species evolving plant‐dominated diets evolved deeper incisors, longer third molars, longer molar crests, blunter posteriorly angled cusps, and more expanded laterally oriented occlusal cusps than species adapting to animal‐dominated diets. Measures of incisor depth, crest length, cusp angle and sharpness, occlusal cusp orientation, and the lengths of third molars proved the best predictors of dietary adaptation. Accounting for evolutionary history in a phylogenetic discriminant function analysis notably improved the classification accuracy. Molar morphology is strongly correlated with diet and we suggest that these dental traits can be used to infer diet with good accuracy for both extinct and extant murine species.     

Review. The multiple roles of cultural transmission experiments in understanding human cultural evolution

In this paper, we explore how experimental studies of cultural transmission in adult humans can address general questions regarding the 'who, what, when and how' of human cultural transmission, and consequently inform a theory of human cultural evolution. Three methods are discussed. The transmission chain method, in which information is passed along linear chains of participants, has been used to identify content biases in cultural transmission. These concern the kind of information that is transmitted. Several such candidate content biases have now emerged from the experimental literature. The replacement method, in which participants in groups are gradually replaced or moved across groups, has been used to study phenomena such as cumulative cultural evolution, cultural group selection and cultural innovation. The closed-group method, in which participants learn in groups with no replacement, has been used to explore issues such as who people choose to learn from and when they learn culturally as opposed to individually. A number of the studies reviewed here have received relatively little attention within their own disciplines, but we suggest that these, and future experimental studies of cultural transmission that build on them, can play an important role in a broader science of cultural evolution.     

Higher frequency of social learning in China than in the West shows cultural variation in the dynamics of cultural evolution

Cultural evolutionary models have identified a range of conditions under which social learning (copying others) is predicted to be adaptive relative to asocial learning (learning on one''s own), particularly in humans where socially learned information can accumulate over successive generations. However, cultural evolution and behavioural economics experiments have consistently shown apparently maladaptive under-utilization of social information in Western populations. Here we provide experimental evidence of cultural variation in people''s use of social learning, potentially explaining this mismatch. People in mainland China showed significantly more social learning than British people in an artefact-design task designed to assess the adaptiveness of social information use. People in Hong Kong, and Chinese immigrants in the UK, resembled British people in their social information use, suggesting a recent shift in these groups from social to asocial learning due to exposure to Western culture. Finally, Chinese mainland participants responded less than other participants to increased environmental change within the task. Our results suggest that learning strategies in humans are culturally variable and not genetically fixed, necessitating the study of the ‘social learning of social learning strategies'' whereby the dynamics of cultural evolution are responsive to social processes, such as migration, education and globalization.     

Updated imaging and phylogenetic comparative methods reassess relative temporal lobe size in anthropoids and modern humans

Objectives

Two decades ago, Rilling and Seligman, hereafter abbreviated to RAS Study, suggested modern humans had relatively larger temporal lobes for brain size compared to other anthropoids. Despite many subsequent studies drawing conclusions about the evolutionary implications for the emergence of unique cerebral specializations in Homo sapiens, no re-assessment has occurred using updated methodologies.

Methods

We reassessed the association between right temporal lobe volume (TLV) and right hemisphere volume (HV) in the anthropoid brain. In a sample compiled de novo by us, T1-weighted in vivo Magnetic Resonance Imaging (MRI) scans of 11 extant anthropoid species were calculated by-voxel from the MRI and the raw data from RAS Study directly compared to our sample. Phylogenetic Generalized Least-Squares (PGLS) regression and trait-mapping using Blomberg's K (kappa) tested the correlation between HV and TLV accounting for anthropoid phylogeny, while bootstrapped PGLS regressions tested difference in slopes and intercepts between monkey and ape subsamples.

Results

PGLS regressions indicated statistically significant correlations (r² < 0.99; p ≤ 0.0001) between TLV and HV with moderate influence from phylogeny (K ≤ 0.42). Bootstrapped PGLS regression did not show statistically significant differences in slopes between monkeys and apes but did for intercepts. In our sample, human TLV was not larger than expected for anthropoids.

Discussion

Updated imaging, increased sample size and advanced statistical analyses did not find statistically significant results that modern humans possessed a disproportionately large temporal lobe volume compared to the general anthropoid trend. This has important implications for human and non-human primate brain evolution.     

Discrete and morphometric traits reveal contrasting patterns and processes in the macroevolutionary history of a clade of scorpions

Many palaeontological studies have investigated the evolution of entire body plans, generally relying on discrete character‐taxon matrices. In contrast, macroevolutionary studies performed by neontologists have mostly focused on morphometric traits. Although these data types are very different, some studies have suggested that they capture common patterns. Nonetheless, the tests employed to support this claim have not explicitly incorporated a phylogenetic framework and may therefore be susceptible to confounding effects due to the presence of common phylogenetic structure. We address this question using the scorpion genus Brachistosternus Pocock 1893 as case study. We make use of a time‐calibrated multilocus molecular phylogeny, and compile discrete and traditional morphometric data sets, both capturing the overall morphology of the organisms. We find that morphospaces derived from these matrices are significantly different, and that the degree of discordance cannot be replicated by simulations of random character evolution. Moreover, we find strong support for contrasting modes of evolution, with discrete characters being congruent with an ‘early burst’ scenario whereas morphometric traits suggest species‐specific adaptations to have driven morphological evolution. The inferred macroevolutionary dynamics are therefore contingent on the choice of character type. Finally, we confirm that metrics of correlation fail to detect these profound differences given common phylogenetic structure in both data sets, and that methods incorporating a phylogenetic framework and accounting for expected covariance should be favoured.     

Coordination between leaf and root traits in Mediterranean coastal dune plants

• Plant trait-based functional spectra are crucial to assess ecosystem functions and services. Whilst most research has focused on aboveground vegetative traits (leaf economic spectrum, LES), contrasting evidence on any coordination between the LES and root economic spectrum (RES) has been reported. Studying spectra variation along environmental gradients and accounting for species' phylogenetic relatedness may help to elucidate the strength of coordination between above- and belowground trait variation.
• We focused on leaf and root traits of 39 species sampled in three distinct habitats (front, back and slack) along a shoreline–inland gradient on coastal dunes. We tested, within a phylogenetic comparative framework, for the presence of the LES and RES, for any coordination between these spectra, and explored their relation to variation in ecological strategies along this gradient.
• In each habitat, three-quarters of trait variation is captured in two-dimensional spectra, with species' phylogenetic relatedness moderately influencing coordination and trade-off between traits. Along the shoreline–inland gradient, aboveground traits support the LES in all habitats. Belowground traits are consistent with the RES in the back-habitat only, where the environmental constraints are weaker, and a coordination between leaf and root traits was also found, supporting the whole-plant spectrum (PES).
• This study confirms the complexity when seeking any correlation between the LES and RES in ecosystems characterized by multiple environmental pressures, such as those investigated here. Changes in traits adopted to resist environmental constraints are similar among species, independent of their evolutionary relatedness, thus explaining the low phylogenetic contribution in support of our results.

     

Adjacent chromosomal regions can evolve at very different rates: Evolution of theDrosophila 68C glue gene cluster

Summary The 68C puff is a highly transcribed region of theDrosophila melanogaster salivary gland polytene chromosomes. Three different classes of messenger RNA originate in a 5000-bp region in the puff; each class is translated to one of the salivary gland glue proteins sgs-3, sgs-7, or sgs-8. These messenger RNA classes are coordinately controlled, with each RNA appearing in the third larval instar and disappearing at the time of puparium formation. Their disappearance is initiated by the action of the steroid hormone ecdysterone. In the work reported here, we studied evolution of this hormone-regulated gene cluster in themelanogaster species subgroup ofDrosophila. Genome blot hybridization experiments showed that five other species of this subgroup have DNA sequences that hybridize toD. melanogaster 68C sequences, and that these sequences are divided into a highly conserved region, which does not contain the glue genes, and an extraordinarily diverged region, which does. Molecular cloning of this DNA fromD. simulans, D. erecta, D. yakuba, andD. teissieri confirmed the division of the region into a slowly and a rapidly evolving protion, and also showed that the rapidly evolving region of each species codes for third instar larval salivary gland RNAs homologous to theD. melanogaster glue mRNAs. The highly conserved region is at least 13,000 bp long, and is not known to code for any RNAs.     

Evolution of altitudinal migration in passerines is linked to diet

Bird migration is typically associated with a latitudinal movement from north to south and vice versa. However, many bird species migrate seasonally with an upslope or downslope movement in a process termed altitudinal migration. Globally, 830 of the 6,579 Passeriformes species are considered altitudinal migrants and this pattern has emerged multiple times across 77 families of this order. Recent work has indicated an association between altitudinal migration and diet, but none have looked at diet as a potential evolutionary driver. Here, we investigated potential evolutionary drivers of altitudinal migration in passerines around the world by using phylogenetic comparative methods. We tested for evolutionary associations between altitudinal migration and foraging guild and primary habitat preference in passerines species worldwide. Our results indicate that foraging guild is evolutionarily associated with altitudinal migration, but this relationship varies across zoogeographical regions. In the Nearctic, herbivorous and omnivorous species are associated with altitudinal migration, while only omnivorous species are associated with altitudinal migration in the Palearctic. Habitat was not strongly linked to the evolution of altitudinal migration. While our results point to diet as a potentially important driver of altitudinal migration, the evolution of this behavior is complex and certainly driven by multiple factors. Altitudinal migration varies in its use (for breeding or molting), within a species, population, and even at the individual level. As such, the evolution of altitudinal migration is likely driven by an ensemble of factors, but this study provides a beginning framework for understanding the evolution of this complex behavior.     

Relative rates of evolution in the coding and control regions of African mtDNAs

Reduced median networks of African haplogroup L mitochondrial DNA (mtDNA) sequences were analyzed to determine the pattern of substitutions in both the noncoding control and coding regions. In particular, we attempted to determine the causes of the previously reported (Howell et al. 2004) violation of the molecular clock during the evolution of these sequences. In the coding region, there was a significantly higher rate of substitution at synonymous sites than at nonsynonymous sites as well as in the tRNA and rRNA genes. This is further evidence for the operation of purifying selection during human mtDNA evolution. For most sites in the control region, the relative rate of substitution was similar to the rate of neutral evolution (assumed to be most closely approximated by the substitution rate at 4-fold degenerate sites). However, there are a number of mutational hot spots in the control region, approximately 3% of the total sites, that have a rate of substitution greater than the neutral rate, at some sites by more than an order of magnitude. It is possible either that these sites are evolving under conditions of positive selection or that the substitution rate at some sites in the control region is strongly dependent upon sequence context. Finally, we obtained preliminary evidence for "nonideal" evolution in the control region, including haplogroup-specific substitution patterns and a decoupling between relative rates of substitution in the control and coding regions.     

The monophyletic origin of delayed implantation in carnivores and its implications

Abstract. In several carnivores a newly fertilized egg enters diapause instead of being directly implanted into the uterus, a phenomenon called delayed implantation. Several hypotheses have been forwarded to explain the utility of this prolonged gestation period, but all of these depend on several independent origins of the character. Here, we conduct a phylogenetic reconstruction of the evolution of delayed implantation in the Carnivora that reveals one basal origin, with additional transitions all having occurred within the Mustelidae. Hence, previous hypotheses relating to its evolution become untestable. Further analyses revealed that the presence or absence of delayed implantation is unrelated to the timing of mating season and birth season. Instead, mustelids with direct implantation are smaller than those with delayed implantation. We therefore suggest that delayed implantation has been selected against in small species due to the relatively higher fecundity costs of a prolonged gestation period.