How to treat mixed behavior segments in supervised machine learning of behavioural modes from inertial measurement data.

The application of supervised machine learning methods to identify behavioural modes from inertial measurements of bio-loggers has become a standard tool in behavioural ecology. Several design choices can affect the accuracy of identifying the behavioural modes. One such choice is the inclusion or exclusion of segments consisting of more than a single behaviour (mixed segments) in the machine learning model training data. Currently, the common practice is to ignore such segments during model training. In this paper we tested the hypothesis that including mixed segments in model training will improve accuracy, as the model would perform better in identifying them in the test data. We test this hypothesis using a series of data simulations on four datasets of accelerometer data coupled with behaviour observations, obtained from four study species (Damaraland mole-rats, meerkats, olive baboons, polar bears). Results show that when a substantial proportion of the test data are mixed behaviour segments (above ~ 10%), including mixed segments in machine learning model training improves the accuracy of classification. These results were consistent across the four study species, and robust to changes in segment length, sample size, and degree of mixture within the mixed segments. However, we also find that in some cases (particularly in baboons) models trained with mixed segments show reduced accuracy in classifying test data containing only single behaviour (pure) segments, compared to models trained without mixed segments. Based on these results, we recommend that when the classification model is expected to deal with a substantial proportion of mixed behaviour segments (> 10%), it is beneficial to include them in model training, otherwise, it is unnecessary but also not harmful. The exception is when there is a basis to assume that the training data contains a higher rate of mixed segments than the actual (unobserved) data to be classified-such a situation may occur particularly when training data are collected in captivity and used to classify data from the wild. In this case, excess inclusion of mixed segments in training data should probably be avoided.

Thiamin dynamics during the adult life cycle of Atlantic salmon (Salmo salar).

Thiamin is an essential water-soluble B vitamin known for its wide range of metabolic functions and antioxidant properties. Over the past decades, reproductive failures induced by thiamin deficiency have been observed in several salmonid species worldwide, but it is unclear why this micronutrient deficiency arises. Few studies have compared thiamin concentrations in systems of salmonid populations with or without documented thiamin deficiency. Moreover, it is not well known whether and how thiamin concentration changes during the marine feeding phase and the spawning migration. Therefore, samples of Atlantic salmon (Salmo salar) were collected when actively feeding in the open Baltic Sea, after the sea migration to natal rivers, after river migration, and during the spawning period. To compare populations of Baltic salmon with systems without documented thiamin deficiency, a population of landlocked salmon located in Lake Vänern (Sweden) was sampled as well as salmon from Norwegian rivers draining into the North Atlantic Ocean. Results showed the highest mean thiamin concentrations in Lake Vänern salmon, followed by North Atlantic, and the lowest in Baltic populations. Therefore, salmon in the Baltic Sea seem to be consistently more constrained by thiamin than those in other systems. Condition factor and body length had little to no effect on thiamin concentrations in all systems, suggesting that there is no relation between the body condition of salmon and thiamin deficiency. In our large spatiotemporal comparison of salmon populations, thiamin concentrations declined toward spawning in all studied systems, suggesting that the reduction in thiamin concentration arises as a natural consequence of starvation rather than to be related to thiamin deficiency in the system. These results suggest that factors affecting accumulation during the marine feeding phase are key for understanding the thiamin deficiency in salmonids.

Phylogenetic modeling of enhancer shifts in African mole-rats reveals regulatory changes associated with tissue-specific traits.

Changes in gene regulation are thought to underlie most phenotypic differences between species. For subterranean rodents such as the naked mole-rat, proposed phenotypic adaptations include hypoxia tolerance, metabolic changes, and cancer resistance. However, it is largely unknown what regulatory changes may associate with these phenotypic traits, and whether these are unique to the naked mole-rat, the mole-rat clade, or are also present in other mammals. Here, we investigate regulatory evolution in the heart and liver from two African mole-rat species and two rodent outgroups using genome-wide epigenomic profiling. First, we adapted and applied a phylogenetic modeling approach to quantitatively compare epigenomic signals at orthologous regulatory elements and identified thousands of promoter and enhancer regions with differential epigenomic activity in mole-rats. These elements associate with known mole-rat adaptations in metabolic and functional pathways and suggest candidate genetic loci that may underlie mole-rat innovations. Second, we evaluated ancestral and species-specific regulatory changes in the study phylogeny and report several candidate pathways experiencing stepwise remodeling during the evolution of mole-rats, such as the insulin and hypoxia response pathways. Third, we report nonorthologous regulatory elements overlap with lineage-specific repetitive elements and appear to modify metabolic pathways by rewiring of HNF4 and RAR/RXR transcription factor binding sites in mole-rats. These comparative analyses reveal how mole-rat regulatory evolution informs previously reported phenotypic adaptations. Moreover, the phylogenetic modeling framework we propose here improves upon the state of the art by addressing known limitations of inter-species comparisons of epigenomic profiles and has broad implications in the field of comparative functional genomics.

Environmental effects rather than relatedness determine gut microbiome similarity in a social mammal.

In social species, group members commonly show substantial similarity in gut microbiome composition. Such similarities have been hypothesized to arise either by shared environmental effects or by host relatedness. However, disentangling these factors is difficult, because group members are often related, and social groups typically share similar environmental conditions. In this study, we conducted a cross-foster experiment under controlled laboratory conditions in group-living Damaraland mole-rats (Fukomys damarensis) and used 16S amplicon sequencing to disentangle the effects of the environment and relatedness on gut microbiome similarity and diversity. Our results show that a shared environment is the main factor explaining gut microbiome similarity, overshadowing any effect of host relatedness. Together with studies in wild animal populations, our results suggest that among conspecifics environmental factors are more powerful drivers of gut microbiome composition similarity than host genetics.

Damaraland mole-rats do not rely on helpers for reproduction or survival.

In eusocial invertebrates and obligate cooperative breeders, successful reproduction is dependent on assistance from non-breeding group members. Although naked (Heterocephalus glaber) and Damaraland mole-rats (Fukomys damarensis) are often described as eusocial and their groups are suggested to resemble those of eusocial insects more closely than groups of any other vertebrate, the extent to which breeding individuals benefit from the assistance of non-breeding group members is unclear. Here we show that, in wild Damaraland mole-rats, prospective female breeders usually disperse and settle alone in new burrow systems where they show high survival rates and remain in good body condition-often for several years-before being joined by males. In contrast to many obligate cooperative vertebrates, pairs reproduced successfully without non-breeding helpers, and the breeding success of experimentally formed pairs was similar to that of larger, established groups. Though larger breeding groups recruited slightly more pups than smaller groups, adult survival was independent of group size and group size had mixed effects on the growth of non-breeders. Our results suggest that Damaraland mole-rats do not need groups to survive and that cooperative breeding in the species is not obligate as pairs can-and frequently do-reproduce without the assistance of helpers. While re-emphasizing the importance of ecological constraints on dispersal in social mole-rats, the mixed effects of group size in our study suggest that indirect benefits accrued through cooperative behavior may have played a less prominent role in the evolution of mole-rat group-living than previously thought.

Coercion promotes alloparental care in cooperative breeders.

Members of social groups may negotiate among each other about the exchange of goods and services. If this involves asymmetries between interacting partners, for instance in condition, power, or expected payoffs, coercion may be involved in the bargain. Cooperative breeders are excellent models to study such interactions, because asymmetries are inherent in the relationship between dominant breeders and subordinate helpers. Currently it is unclear whether punishment is used to enforce costly cooperation in such systems. Here we investigated experimentally in the cooperatively breeding cichlid Neolamprologus pulcher whether alloparental brood care provided by subordinates is contingent on enforcement by dominant breeders. We manipulated first the brood care behavior of a subordinate group member and then the possibility of the dominant breeders to punish idle helpers. When subordinates were prevented from providing brood care, breeders increased their attacks on them, which triggered increased alloparental brood care by helpers as soon as this was again possible. In contrast, when the possibility to punish helpers was prevented, energetically costly alloparental brood care did not increase. Our results confirm predictions of the pay-to-stay mechanism causing alloparental care in this species and they suggest more generally that coercion can play an important role in the control of cooperation.

Philopatry yields higher fitness than dispersal in a cooperative breeder with sex-specific life history trajectories.

Social evolution is tightly linked to dispersal decisions, but the ecological and social factors selecting for philopatry or dispersal often remain obscure. Elucidating selection mechanisms underlying alternative life histories requires measurement of fitness effects in the wild. We report on a long-term field study of 496 individually marked cooperatively breeding fish, showing that philopatry is beneficial as it increases breeding tenure and lifetime reproductive success in both sexes. Dispersers predominantly join established groups and end up in smaller groups when they ascend to dominance. Life history trajectories are sex specific, with males growing faster, dying earlier, and dispersing more, whereas females more likely inherit a breeding position. Increased male dispersal does not seem to reflect an adaptive preference but rather sex-specific differences in intrasexual competition. Cooperative groups may thus be maintained because of inherent benefits of philopatry, of which females seem to get the greater share in social cichlids.

Bacteroidetes to Firmicutes: captivity changes the gut microbiota composition and diversity in a social subterranean rodent.

BACKGROUND: In mammals, the gut microbiota has important effects on the health of their hosts. Recent research highlights that animal populations that live in captivity often differ in microbiota diversity and composition from wild populations. However, the changes that may occur when animals move to captivity remain difficult to predict and factors generating such differences are poorly understood. Here we compare the bacterial gut microbiota of wild and captive Damaraland mole-rats (Fukomys damarensis) originating from a population in the southern Kalahari Desert to characterise the changes of the gut microbiota that occur from one generation to the next generation in a long-lived, social rodent species. RESULTS: We found a clear divergence in the composition of the gut microbiota of captive and wild Damaraland mole-rats. Although the dominating higher-rank bacterial taxa were the same in the two groups, captive animals had an increased ratio of relative abundance of Firmicutes to Bacteroidetes compared to wild animals. The Amplicon Sequence Variants (ASVs) that were strongly associated with wild animals were commonly members of the same bacterial families as those strongly associated with captive animals. Captive animals had much higher ASV richness compared to wild-caught animals, explained by an increased richness within the Firmicutes. CONCLUSION: We found that the gut microbiota of captive hosts differs substantially from the gut microbiota composition of wild hosts. The largest differences between the two groups were found in shifts in relative abundances and diversity of Firmicutes and Bacteroidetes.

Freeze-drying can replace cold-chains for transport and storage of fecal microbiome samples.

Background: The transport and storage of samples in temperatures of minus 80 °C is commonly considered as the gold standard for microbiome studies. However, studies conducting sample collection at remote sites without a reliable cold-chain would benefit from a sample preservation method that allows transport and storage at ambient temperature. Methods: In this study we compare alpha diversity and 16S microbiome composition of 20 fecal sample replicates from Damaraland mole-rats (Fukomys damarensis) preserved in a minus 80 °C freezer and transported on dry ice to freeze-dried samples that were stored and transported in ambient temperature until DNA extraction. Results: We found strong correlations between relative abundances of Amplicon Sequence Variants (ASVs) between preservation treatments of the sample, no differences in alpha diversity measures between the two preservation treatments and minor effects of the preservation treatment on beta diversity measures. Our results show that freeze-drying samples can be a useful method for cost-effective transportation and storage of microbiome samples that yields quantitatively almost indistinguishable results in 16S microbiome analyses as those stored in minus 80 °C.

Increases in glucocorticoids are sufficient but not necessary to increase cooperative burrowing in Damaraland mole-rats.

Despite widespread interest in the evolution of cooperative behaviour, the physiological mechanisms shaping their expression remain elusive. We tested the hypothesis that glucocorticoid (GC) hormones affect cooperative behaviour using captive Damaraland mole-rats (Fukomys damarensis), a cooperatively breeding mammal. Within groups, individuals routinely contribute to public goods that include foraging tunnels, which provide all group members access to the tubers of desert plants they feed on, communal food stores and nests. We found that experimental increases in glucocorticoid concentration (GCc) in non-breeding female helpers led them to be active for longer and to burrow more while active, raising their daily contributions to burrowing, but not food carrying or nest building. However, experimentally induced increases in burrowing did not lead to elevated GCc in helpers of both sexes. These results suggest that heightened GCc may stimulate some cooperative behaviours that are energetically demanding (a characteristic shared by many types of cooperative activities across species) but that the cooperative behaviours affected by GCc can also be regulated by other mechanisms.

Breeders are less active foragers than non-breeders in wild Damaraland mole-rats.

Eusocial societies are characterized by a clear division of labour between non-breeding workers and breeding queens, and queens often do not contribute to foraging, defence and other maintenance tasks. It has been suggested that the structure and organization of social mole-rat groups resembles that of eusocial insect societies. However, the division of labour has rarely been investigated in wild mole-rats, and it is unknown whether breeders show decreased foraging activity compared with non-breeding helpers in natural groups. Here, we show that, in wild Damaraland mole-rats (Fukomys damarensis), breeders show lower activity in foraging areas than non-breeding group members. Both breeders and non-breeders displayed variation in activity across the different seasons. Our results suggest that group living allows social mole-rat breeders to reduce their investment in energetically costly behaviour, or alternatively, that the high cost of reproduction in this species forces a behavioural trade-off against foraging investment.

No task specialization among helpers in Damaraland mole-rats.

The specialization of individuals in specific behavioural tasks is often attributed either to irreversible differences in development, which generate functionally divergent cooperative phenotypes, or to age-related changes in the relative frequency with which individuals perform different cooperative activities; both of which are common in many insect caste systems. However, contrasts in cooperative behaviour can take other forms and, to date, few studies of cooperative behaviour in vertebrates have explored the effects of age, adult phenotype and early development on individual differences in cooperative behaviour in sufficient detail to discriminate between these alternatives. Here, we used multinomial models to quantify the extent of behavioural specialization within nonreproductive Damaraland mole-rats, Fukomys damarensis, at different ages. We showed that, although there were large differences between individuals in their contribution to cooperative activities, there was no evidence of individual specialization in cooperative activities that resembled the differences found in insect societies with distinct castes where individual contributions to different activities are negatively related to each other. Instead, individual differences in helping behaviour appeared to be the result of age-related changes in the extent to which individuals committed to all forms of helping. A similar pattern is observed in cooperatively breeding meerkats, Suricata suricatta, and there is no unequivocal evidence of caste differentiation in any cooperative vertebrate. The multinomial models we employed offer a powerful heuristic tool to explore task specialization and developmental divergence across social taxa and provide an analytical approach that may be useful in exploring the distribution of different forms of helping behaviour in other cooperative species.

Reproduction triggers adaptive increases in body size in female mole-rats.

In social mole-rats, breeding females are larger and more elongated than non-breeding female helpers. This status-related morphological divergence is thought to arise from modifications of skeletal growth following the death or removal of the previous breeder and the transition of their successors from a non-breeding to a breeding role. However, it is not clear what changes in growth are involved, whether they are stimulated by the relaxation of reproductive suppression or by changes in breeding status, or whether they are associated with fecundity increases. Here, we show that, in captive Damaraland mole-rats (Fukomys damarensis), where breeding was experimentally controlled in age-matched siblings, individuals changed in size and shape through a lengthening of the lumbar vertebrae when they began breeding. This skeletal remodelling results from changes in breeding status because (i) females removed from a group setting and placed solitarily showed no increases in growth and (ii) females dispersing from natural groups that have not yet bred do not differ in size and shape from helpers in established groups. Growth patterns consequently resemble other social vertebrates where contrasts in size and shape follow the acquisition of the breeding role. Our results also suggest that the increases in female body size provide fecundity benefits. Similar forms of socially responsive growth might be more prevalent in vertebrates than is currently recognized, but the extent to which this is the case, and the implications for the structuring of mammalian dominance hierarchies, are as yet poorly understood.

Allo-parental care in Damaraland mole-rats is female biased and age dependent, though independent of testosterone levels.

In Damaraland mole-rats (Fukomys damarensis), non-breeding subordinates contribute to the care of offspring born to the breeding pair in their group by carrying and retrieving young to the nest. In social mole-rats and some cooperative breeders, dominant females show unusually high testosterone levels and it has been suggested that high testosterone levels may increase reproductive and aggressive behavior and reduce investment in allo-parental and parental care, generating age and state-dependent variation in behavior. Here we show that, in Damaraland mole-rats, allo-parental care in males and females is unaffected by experimental increases in testosterone levels. Pup carrying decreases with age of the non-breeding helper while the change in social status from non-breeder to breeder has contrasting effects in the two sexes. Female breeders were more likely than female non-breeders to carry pups but male breeders were less likely to carry pups than male non-breeders, increasing the sex bias in parental care compared to allo-parental care. Our results indicate that testosterone is unlikely to be an important regulator of allo-parental care in mole-rats.

Growth affects dispersal success in social mole-rats, but not the duration of philopatry.

In naked mole-rats (Heterocephalus glaber), some non-breeding males show faster growth and are more likely to disperse than others. These differences have been suggested to be the result of a specialized developmental strategy leading to shorter philopatry and independent breeding, as opposed to extended philopatry as non-reproductive helpers. However, it is unclear whether fast-growing males disperse sooner than slow-growing males. An alternative explanation is that variation in quality between individuals causes high-quality individuals to grow quickly and maximize dispersal success without reducing philopatry. Here we show that in Damaraland mole-rats (Fukomys damarensis), males that subsequently disperse successfully grow faster than other non-reproductive males. This pattern is predicted by both hypotheses and does not discriminate between them. However, contrary to the suggestion that faster growth represents a developmental specialization for early dispersal, fast-growing and slow-growing males remained equally long in their natal groups. Our study provides no evidence for adaptive divergence in male development leading either to early dispersal or extended philopatry. Instead of representing specialized dispersers, fast-growing males of this species may be high-quality individuals.

Variation in growth of Damaraland mole-rats is explained by competition rather than by functional specialization for different tasks.

In some eusocial insect societies, adaptation to the division of labour results in multimodal size variation among workers. It has been suggested that variation in size and growth among non-breeders in naked and Damaraland mole-rats may similarly reflect functional divergence associated with different cooperative tasks. However, it is unclear whether individual growth rates are multimodally distributed (as would be expected if variation in growth is associated with specialization for different tasks) or whether variation in growth is unimodally distributed, and is related to differences in the social and physical environment (as would be predicted if there are individual differences in growth but no discrete differences in developmental pathways). Here, we show that growth trajectories of non-breeding Damaraland mole-rats vary widely, and that their distribution is unimodal, contrary to the suggestion that variation in growth is the result of differentiation into discrete castes. Though there is no evidence of discrete variation in growth, social factors appear to exert important effects on growth rates and age-specific size, which are both reduced in large social groups.

Differences in cooperative behavior among Damaraland mole rats are consequences of an age-related polyethism.

In many cooperative breeders, the contributions of helpers to cooperative activities change with age, resulting in age-related polyethisms. In contrast, some studies of social mole rats (including naked mole rats, Heterocephalus glaber, and Damaraland mole rats, Fukomys damarensis) suggest that individual differences in cooperative behavior are the result of divergent developmental pathways, leading to discrete and permanent functional categories of helpers that resemble the caste systems found in eusocial insects. Here we show that, in Damaraland mole rats, individual contributions to cooperative behavior increase with age and are higher in fast-growing individuals. Individual contributions to different cooperative tasks are intercorrelated and repeatability of cooperative behavior is similar to that found in other cooperatively breeding vertebrates. Our data provide no evidence that nonreproductive individuals show divergent developmental pathways or specialize in particular tasks. Instead of representing a caste system, variation in the behavior of nonreproductive individuals in Damaraland mole rats closely resembles that found in other cooperatively breeding mammals and appears to be a consequence of age-related polyethism.

Invasive parasites, habitat change and heavy rainfall reduce breeding success in Darwin's finches.

Invasive alien parasites and pathogens are a growing threat to biodiversity worldwide, which can contribute to the extinction of endemic species. On the Galápagos Islands, the invasive parasitic fly Philornis downsi poses a major threat to the endemic avifauna. Here, we investigated the influence of this parasite on the breeding success of two Darwin's finch species, the warbler finch (Certhidea olivacea) and the sympatric small tree finch (Camarhynchus parvulus), on Santa Cruz Island in 2010 and 2012. While the population of the small tree finch appeared to be stable, the warbler finch has experienced a dramatic decline in population size on Santa Cruz Island since 1997. We aimed to identify whether warbler finches are particularly vulnerable during different stages of the breeding cycle. Contrary to our prediction, breeding success was lower in the small tree finch than in the warbler finch. In both species P. downsi had a strong negative impact on breeding success and our data suggest that heavy rain events also lowered the fledging success. On the one hand parents might be less efficient in compensating their chicks' energy loss due to parasitism as they might be less efficient in foraging on days of heavy rain. On the other hand, intense rainfalls might lead to increased humidity and more rapid cooling of the nests. In the case of the warbler finch we found that the control of invasive plant species with herbicides had a significant additive negative impact on the breeding success. It is very likely that the availability of insects (i.e. food abundance)is lower in such controlled areas, as herbicide usage led to the removal of the entire understory. Predation seems to be a minor factor in brood loss.

Group-size-dependent punishment of idle subordinates in a cooperative breeder where helpers pay to stay.

In cooperative breeding systems, dominant breeders sometimes tolerate unrelated individuals even if they inflict costs on the dominants. According to the 'pay-to-stay' hypothesis, (i) subordinates can outweigh these costs by providing help and (ii) dominants should be able to enforce help by punishing subordinates that provide insufficient help. This requires that dominants can monitor helping and can recognize group members individually. In a field experiment, we tested whether cooperatively breeding cichlid Neolamprologus pulcher subordinates increase their help after a forced 'idle' period, how other group members respond to a previously idle helper, and how helper behaviour and group responses depend on group size. Previously, idle helpers increased their submissiveness and received more aggression than control helpers, suggesting that punishment occurred to enforce help. Subordinates in small groups increased their help more than those in large groups, despite receiving less aggression. When subordinates were temporarily removed, dominants in small groups were more likely to evict returning subordinates. Our results suggest that only in small groups do helpers face a latent threat of punishment by breeders as predicted by the pay-to-stay hypothesis. In large groups, cognitive constraints may prevent breeders from tracking the behaviour of a large number of helpers.