Sarah J. Hodge

Dynamic Analyses of the Expression of the HISTONE::YFP Fusion Protein in Arabidopsis Show That Syncytial Endosperm Is Divided in Mitotic Domains

During early seed development, nuclear divisions in the endosperm are not followed by cell division, leading to the development of a syncytium. The simple organization of the Arabidopsis endosperm provides a model in which to study the regulation of the cell cycle in relation to development. To monitor nuclear divisions, we constructed a HISTONE 2B::YELLOW FLUORESCENT PROTEIN gene fusion (H2B::YFP). To validate its use as a vital marker for chromatin in plants, H2B::YFP was expressed constitutively in Arabidopsis. This enabled the observation of mitoses in living root meristems. H2B::YFP was expressed specifically in Arabidopsis syncytial endosperm by using GAL4 transactivation. Monitoring mitotic activity in living syncytial endosperm showed that the syncytium was organized into three domains in which nuclei divide simultaneously with a specific time course. Each mitotic domain has a distinct spatiotemporal pattern of mitotic CYCLIN B1;1 accumulation. The polar spatial organization of the three mitotic domains suggests interactions between developmental mechanisms and the regulation of the cell cycle.

Intrasexual competition and sexual selection in cooperative mammals

In most animals, the sex that invests least in its offspring competes more intensely for access to the opposite sex and shows greater development of secondary sexual characters than the sex that invests most. However, in some mammals where females are the primary care-givers, females compete more frequently or intensely with each other than males. A possible explanation is that, in these species, the resources necessary for successful female reproduction are heavily concentrated and intrasexual competition for breeding opportunities is more intense among females than among males. Intrasexual competition between females is likely to be particularly intense in cooperative breeders where a single female monopolizes reproduction in each group. Here, we use data from a twelve-year study of wild meerkats (Suricata suricatta), where females show high levels of reproductive skew, to show that females gain greater benefits from acquiring dominant status than males and traits that increase competitive ability exert a stronger influence on their breeding success. Females that acquire dominant status also develop a suite of morphological, physiological and behavioural characteristics that help them to control other group members. Our results show that sex differences in parental investment are not the only mechanism capable of generating sex differences in reproductive competition and emphasize the extent to which competition for breeding opportunities between females can affect the evolution of sex differences and the operation of sexual selection.

Reproductive control via eviction (but not the threat of eviction) in banded mongooses.

Considerable research has focused on understanding variation in reproductive skew in cooperative animal societies, but the pace of theoretical development has far outstripped empirical testing of the models. One major class of model suggests that dominant individuals can use the threat of eviction to deter subordinate reproduction (the ‘restraint’ model), but this idea remains untested. Here, we use long-term behavioural and genetic data to test the assumptions of the restraint model in banded mongooses (Mungos mungo), a species in which subordinates breed regularly and evictions are common. We found that dominant females suffer reproductive costs when subordinates breed, and respond to these costs by evicting breeding subordinates from the group en masse, in agreement with the assumptions of the model. We found no evidence, however, that subordinate females exercise reproductive restraint to avoid being evicted in the first place. This means that the pattern of reproduction is not the result of a reproductive ‘transaction’ to avert the threat of eviction. We present a simple game theoretical analysis that suggests that eviction threats may often be ineffective to induce pre-emptive restraint among multiple subordinates and predicts that threats of eviction (or departure) will be much more effective in dyadic relationships and linear hierarchies. Transactional models may be more applicable to these systems. Greater focus on testing the assumptions rather than predictions of skew models can lead to a better understanding of how animals control each others reproduction, and the extent to which behaviour is shaped by overt acts versus hidden threats.

A map of KNAT gene expression in the Arabidopsis root.

Homeodomain proteins are key regulators of patterning during the development of animal and plant body plans. Knotted1-like TALE homeodomain proteins have been found to play important roles in the development of the Arabidopsis shoot apical meristem and are part of a complex regulatory network of protein interactions. We have investigated the possible role of the knotted1-like genes KNAT1, KNAT3, KNAT4, and KNAT5 in Arabidopsis root development. Root growth is indeterminate, and the organ shows distinct zones of cell proliferation, elongation and differentiation along its longitudinal axis. Here we show that KNAT1, KNAT3, KNAT4 and KNAT5 show cell type specific expression patterns in the Arabidopsis root. Moreover, they are expressed in different spatially restricted patterns along the longitudinal root axis and in lateral root primordia. Hormones play an important role in maintenance of root growth, and we have studied their effect on KNAT gene expression. We show that KNAT3 expression is repressed by moderate levels of cytokinin. In addition, we show that the subcellular localization of KNAT3 and KNAT4 is regulated, indicating post-translational control of the activities of these transcription factors. The regulated expression of KNAT1, KNAT3, KNAT4 and KNAT5 within the Arabidopsis root suggests a role for these genes in root development. Our data provide the first systematic survey of KNAT gene expression in the Arabidopsis root.

Helpers benefit offspring in both the short and long-term in the cooperatively breeding banded mongoose

Helpers in cooperative and communal breeding species are thought to accrue fitness benefits through improving the condition and survival of the offspring that they care for, yet few studies have shown conclusively that helpers benefit the offspring they rear. Using a novel approach to control for potentially confounding group-specific variables, I compare banded mongoose (Mungos mungo) offspring within the same litter that differ in the amount of time they spend with a helper, and hence the amount of care they receive. I show that pups that spend more time in close proximity to a helper are fed more, grow faster and have a higher probability of survival to independence than their littermates. Moreover, high growth rates during development reduce the age at which females breed for the first time, suggesting that helpers can improve the future fecundity of the offspring for which they care. These results provide strong evidence that it is the amount of investment per se that benefits offspring, rather than some correlate such as territory quality, and validate the assumption that helpers improve the reproductive success of breeders, and hence may gain fitness benefits from their actions. Furthermore, the finding that helpers may benefit offspring in the long-term suggests that current studies underestimate the fitness benefits that helpers gain from rearing the offspring of others.

Factors affecting the reproductive success of dominant male meerkats

Identifying traits that affect the reproductive success of individuals is fundamental for our understanding of evolutionary processes. In cooperative breeders, a dominant male typically restricts mating access to the dominant female for extended periods, resulting in pronounced variation in reproductive success among males. This may result in strong selection for traits that increase the likelihood of dominance acquisition, dominance retention and reproductive rates while dominant. However, despite considerable research on reproductive skew, few studies have explored the factors that influence these three processes among males in cooperative species. Here we use genetic, behavioural and demographic data to investigate the factors affecting reproductive success in dominant male meerkats (Suricata suricatta). Our data show that dominant males sire the majority of all offspring surviving to 1 year. A males likelihood of becoming dominant is strongly influenced by age, but not by weight. Tenure length and reproductive rate, both important components of dominant male reproductive success, are largely affected by group size and composition, rather than individual traits. Dominant males in large groups have longer tenures, but after this effect is controlled, male tenure length also correlates negatively to the number of adult females in the group. Male reproductive rate also declines as the number of intra‐ and extra‐group competitors increases. As the time spent in the dominant position and reproductive rate while dominant explain > 80% of the total variance in reproductive success, group composition thus has major implications for male reproductive success.

Group size and the suppression of subordinate reproduction in Kalahari meerkats

In animal societies, contrasts in reproductive skew among females are caused by variation in the frequency of reproduction by subordinates. However, despite widespread interest in the extent and causes of reproductive skew, few empirical studies have investigated the factors affecting the frequency of successful reproduction by subordinates. We tested the prediction that the extent to which dominants restrict the reproductive success of subordinates should increase as group size rises and the marginal benefits of additional helpers falls. In a long-term study of wild meerkats, Suricata suricatta, we found that dominants were more likely to evict subordinates in large groups than small ones, and that the frequency of breeding by subordinate females declined with group size, largely as a result of increases in abortion rate. The breeding frequency of subordinate females was also influenced by their age and weight, which probably reflects the capability of subordinates to breed and their ability to resist the attempts of dominants to suppress them. These findings highlight the importance of investigating variation in the benefits to dominants of controlling subordinate reproduction as well as variation in the benefits of breeding to subordinate females when attempting to understand variation in subordinate breeding success.

Reproductive competition and the evolution of extreme birth synchrony in a cooperative mammal

Reproductive events in animal societies often show a high degree of temporal clustering, but the evolutionary causes of this synchronization are poorly understood. Here, we suggest that selection to avoid the negative effects of competition with other females has given rise to a remarkable degree of birth synchrony in the communal-breeding banded mongoose (Mungos mungo). Within banded mongoose groups, births are highly synchronous, with 64 per cent of females giving birth on exactly the same night. Our results indicate that this extreme synchrony arises because offspring suffer an increased risk of infanticide if their mother gives birth before other females, but suffer in competition with older littermates if their mother gives birth after them. These findings highlight the important influence that reproductive competition can have for the evolution of reproductive synchrony.

The cost of dominance: suppressing subordinate reproduction affects the reproductive success of dominant female banded mongooses

Social species show considerable variation in the extent to which dominant females suppress subordinate reproduction. Much of this variation may be influenced by the cost of active suppression to dominants, who may be selected to balance the need to maximize the resources available for their own offspring against the costs of interfering with subordinate reproduction. To date, the cost of reproductive suppression has received little attention, despite its potential to influence the outcome of conflict over the distribution of reproduction in social species. Here, we investigate possible costs of reproductive suppression in banded mongooses, where dominant females evict subordinates from their groups, thereby inducing subordinate abortion. We show that evicting subordinate females is associated with substantial costs to dominant females: pups born to females who evicted subordinates while pregnant were lighter than those born after undisturbed gestations; pups whose dependent period was disrupted by an eviction attained a lower weight at independence; and the proportion of a litter that survived to independence was reduced if there was an eviction during the dependent period. To our knowledge, this is the first empirical study indicating a possible cost to dominants in attempting to suppress subordinate breeding, and we argue that much of the variation in reproductive skew both within and between social species may be influenced by adaptive variation in the effort invested in suppression by dominants.

Top males gain high reproductive success by guarding more successful females in a cooperatively breeding mongoose

Of key importance for understanding cooperative societies is the way in which reproductive opportunities are distributed among group members. Traditionally, skew has been thought of as a product of intrasexual competition. However, cooperatively breeding species often live in mixed-sex groups, so the behaviour of one sex has the potential to influence skew in the other. We addressed the importance of inter- and intrasexual conflict in determining reproductive skew through a study of paternity sharing in the cooperatively breeding banded mongoose, Mungus mungo. Unlike banded mongoose females, where reproductive skew is low, males exhibited high skew, with 85% of paternities being assigned to the three oldest males in each group. Individual males appeared unable to monopolize reproduction because females come into oestrus in synchrony and mate multiply. Instead, older males increased their success by mate guarding the oldest, most fecund females. Our findings therefore highlight the importance of mate choice in males and reveal the behavioural differences between the sexes that generate reproductive skew. They also emphasize the considerable influence that female behaviour can have on male reproductive skew.