Singular Breeding Research Articles

Socializing in an Infectious World: The Role of Parasites in Social Evolution of a Unique Rodent Family

Transmission of parasites between hosts is facilitated by close contact of hosts. Consequently, parasites have been proposed as an important constraint to the evolution of sociality accounting for its rarity. Despite the presumed costs associated with parasitism, the majority of species of African mole-rats (Family: Bathyergidae) are social. In fact, only the extremes of sociality (i.e., solitary and singular breeding) are represented in this subterranean rodent family. But how did bathyergids overcome the costs of parasitism? Parasite burden is a function of the exposure and susceptibility of a host to parasites. In this review I explore how living in sealed burrow systems and the group defenses that can be employed by closely related group members can effectively reduce the exposure and susceptibility of social bathyergids to parasites. Evidence suggests that this can be achieved largely by investment in relatively cheap and flexible behavioral rather than physiological defense mechanisms. This also shifts the selection pressure for parasites on successful transmission between group members rather than transmission between groups. In turn, this constrains the evolution of virulence and favors socially transmitted parasites (e.g., mites and lice) further reducing the costs of parasitism for social Bathyergidae. I conclude by highlighting directions for future research to evaluate the mechanisms proposed and to consider parasites as facilitators of social evolution not only in this rodent family but also other singular breeders.

Living on the edge: genetic structure and geographic distribution in the threatened Markham's Storm-Petrel (Hydrobates markhami).

Migratory birds are threatened by habitat loss and degradation, illegal killings, ineffective conservation policies, knowledge gaps and climate change. These threats are particularly troubling in the Procellariiformes (Aves), one of the most endangered bird groups. For “storm-petrels”, their cryptic breeding behavior, asynchrony between populations, and light pollution pose additional threats that contribute to increased mortality.Markham’s Storm-Petrel (Hydrobates markhami), a poorly known migratory species, is a pelagic bird that breeds in dispersed colonies in the Sechura and Atacama Deserts, with asynchronous reproduction between colonies, and is highly affected by artificial lights. Considering its complex conservation scenario and singular breeding, we expected to find narrow habitat distribution conditions, strong geographic genetic structure, and spatially differentiation related to human population activities (e.g., light pollution) and the climate global change. To evaluate these predictions, we analyzed the phylogeography, current and future potential distribution based on mitochondrial gene ND1 and geographic records.The phylogeographic analyses revealed three well-supported clades (i.e., Paracas, Arica, and Salar Grande), and the geographical distribution modeled using an intrinsic conditional model (iCAR) suggests a positive relationship with the mean temperature of the wettest quarter and of the driest quarter, solar radiation, and anthropogenic disturbance. The future predictions under moderate and severe scenarios of global change indicated a drastic distribution area reduction, especially in the southern zone around Tarapacá and Antofagasta in Chile. These suggest a potential loss of unique genetic diversity and the need for conservation actions particularly focused at the edges of the H. markhami distribution.

Monotocy and the evolution of plural breeding in mammals.

In many mammals, breeding females are intolerant of each other and seldom associate closely but, in some, they aggregate in groups that vary in size, stability, and kinship structure. Aggregation frequently increases competition for food, and interspecific differences in female sociality among mammals are commonly attributed to contrasts in ecological parameters, including variation in activity timing, the distribution of resources, as well as the risk of predation. However, there is increasing indication that differences in female sociality are also associated with phylogenetic relationships and with contrasts in life-history parameters. We show here that evolutionary transitions from systems where breeding females usually occupy separate ranges (“singular breeding”) to systems where breeding females usually aggregate (“plural breeding”) have occurred more frequently in monotocous lineages where females produce single young than in polytocous ones where they produce litters. A likely explanation of this association is that competition between breeding females for resources is reduced where they produce single young and is more intense where they produce litters. Our findings reinforce evidence that variation in life-history parameters plays an important role in shaping the evolution of social behavior.

Does sire replacement trigger plural reproduction in matrifilial groups of a singular breeder, Ellobius tancrei?

Group-living species differ in how the reproduction is shared among same-sex individuals and how the reproductive skew is attained. In mammals, the highest level of reproductive skew among females is known for some social African mole-rats. Mole voles (Ellobius, Arvicolinae) are similar to these well-studied subterranean rodents in both ecological specialization and social structure. At present, there is no information about the proximate mechanisms underlying singular breeding in any Ellobius species. In this study of the Zaisan mole voles, E. tancrei, we tested the mother’s influence on reproduction and survival of the young females exposed to an unrelated mate. Nine of 15 daughters housed in pairs bred, and all pairs persisted until the end of the experiment (6 months). The reproduction in the matrifilial trios (n=12) was skewed towards mothers: only one daughter delivered but did not wean the litter. The latency until conception was significantly longer in paired daughters than in mothers from trios. Thus, the reproductive skew in trios may be initially generated by the age or experience difference rather than dominance asymmetry. Only 4 trios persisted for 6 months due to high female mortality. The heavier and older was a mother, and the younger was a daughter at male introduction, the more stable was the trio. The influence of females’ ages on group tenacity may be mediated by the daughter’s age-related reproductive activation. The despotic reproductive monopoly with extreme intolerance between kin reproductive females is unusual for voles and indicates a strong female–female competition in E. tancrei in nature.

Designing Selection Criteria for Use of Reed Canarygrass as a Bioenergy Feedstock

ABSTRACTReed canarygrass (Phalaris arundinacea L.) is a perennial C3 grass with a circumglobal distribution in the Northern Hemisphere and adaptation to a wide range of environmental conditions. This species is currently under development as a bioenergy feedstock in North America and Europe. Thus, the objectives of this study were to (i) quantify genetic variation for biomass quality traits of reed canarygrass cultivars and accessions, (ii) determine the relationships for biomass yield with reed canarygrass quality traits, and (iii) identify favorable and attainable breeding objectives for biomass yield and quality traits of reed canarygrass. Eighty cultivars or accessions were grown at five field locations and evaluated for 26 biomass quality traits in 2006 through 2008. Ignoring biomass quality traits in favor of the singular breeding objective of high biomass yield would be likely to result in a few favorable correlated responses including low N, low ash, low Cl, low Fe, and high enzymatic xylan conversion efficiency. These changes would not be sufficiently large to transform reed canarygrass into a more favorable bioenergy feedstock within a few generations of breeding. To do so will require a more focused effort with a relatively small number of traits, for example, high biomass yield, low ash, and high gross calorific value (GCV) for a thermochemical conversion platform or high biomass yield, low lignin, and high glucan and xylan conversion efficiencies for a fermentation platform.

Suppressing subordinate reproduction provides benefits to dominants in cooperative societies of meerkats.

In many animal societies, a small proportion of dominant females monopolize reproduction by actively suppressing subordinates. Theory assumes that this is because subordinate reproduction depresses the fitness of dominants, yet the effect of subordinate reproduction on dominant behaviour and reproductive success has never been directly assessed. Here, we describe the consequences of experimentally preventing subordinate breeding in 12 groups of wild meerkats (Suricata suricatta) for three breeding attempts, using contraceptive injections. When subordinates are prevented from breeding, dominants are less aggressive towards subordinates and evict them less often, leading to a higher ratio of helpers to dependent pups, and increased provisioning of the dominant’s pups by subordinate females. When subordinate breeding is suppressed, dominants also show improved foraging efficiency, gain more weight during pregnancy and produce heavier pups, which grow faster. These results confirm the benefits of suppression to dominants, and help explain the evolution of singular breeding in vertebrate societies.

Intrasexual competition and female dominance in a singular breeding mammal, the Alpine marmot

Although long neglected, female competition is widespread and may have stronger evolutionary consequences than previously thought. In singular breeders, reproductive success is conditional on social status, and intrasexual competition for the dominant position can be particularly severe in females. Because the ability of females to secure the dominant position may strongly influence their fitness, a better understanding of the determinants of dominance maintenance is needed. Using a 21-year data set on Alpine marmots, Marmota marmota , we investigated the potential drivers of female dominance loss in a singularly breeding mammal. Particularly, we tested whether the dominant females' ability to retain their social position depended on the number and the characteristics (age, relatedness to dominant individuals) of potential competitors in the social unit. To identify the potential underlying mechanism, we further investigated how the number of subordinate females affected females' competitive ability. We found that the risk of losing the dominant position increased with the number of subordinate adult females in the group, but that the age of the subordinate females and their parentage relationships to the dominant individuals were unlikely to be driving dominance loss in this species. Moreover, when the number of potential competitors in the social unit increased, we observed a difference in body mass increase between the dominant and her subordinates leading to a decrease in the body mass difference between dominant females and their subordinate adult females, and ultimately to a higher risk of females losing the dominant position. Overall, our results showed that the number of potential competitors in a social group affects the females' ability to secure their dominant position, and suggested that this effect is mediated through changes in female body mass.

Reproductive success in a low skew, communal breeding mammal: the banded mongoose, Mungos mungo

In most cooperatively breeding species, reproduction is monopolised by a subset of group members. However, in some species most or all individuals breed. The factors that affect reproductive success in such species are vital to understanding why multiple females breed. A key issue is whether or not the presence of other breeders is costly to an individual’s reproductive success. This study examines the factors that affect the post-parturition component of reproductive success in groups of communal-breeding banded mongoose (Mungos mungo), where up to ten females breed together. Per-litter reproductive success was low (only 18% of pups survived from birth to independence). Whilst singular breeding was wholly unsuccessful, there were costs associated with breeding in the presence of increasing numbers of other females and in large groups. Synchronisation of parturition increased litter success, probably because it minimises the opportunity for infanticide or decreases competitive asymmetry between pups born to different females. There was no evidence of inbreeding depression, and reproductive success was generally higher in litters where females only had access to related males within their group. I conclude that communal breeding in female banded mongooses represents a compromise between the benefits of group-living and communal pup care on the one hand, and competition between females to maximise their personal reproductive success on the other. Such conflicts are likely to occur in most communal breeding species. Whilst communal breeding systems are generally considered egalitarian, negative effects of co-breeders on individual reproductive success is still an issue.

Costs and benefits of communal rearing to female prairie voles (Microtus ochrogaster)

Communal rearing of offspring may help mothers maximize their investment in offspring at a reduced cost to their own bodily condition, thus maximizing their potential for reproductive success. The objective of this study was to quantify the costs and benefits of communal rearing to prairie vole (Microtus ochrogaster) pups and mothers. Mothers were assigned to one of three social units: solitary mothers, singularly breeding groups (i.e. one mother and one non-reproductive sister) and plurally breeding groups (i.e. two lactating sisters). For each type of social unit, some replicates were provided with food ad libitum, while others were provided with limited food. The body mass of focal mothers (i.e. the first mother to produce a litter) was a significant predictor of pup growth. Regardless of food availability, litters of focal mothers in plurally breeding groups gained more weight than litters reared by solitary mothers. Pups reared in singularly breeding groups were intermediate in weight gain, but did not gain significantly more weight than solitary offspring. There was no difference in the body mass of focal mothers from each type of social unit, regardless of food availability. Within plurally breeding groups, the weight gain of the two litters and body mass of focal and second mothers did not differ. However, focal mothers from plurally breeding groups nursed fewer pups than solitary mothers and also fewer pups than their nestmates when food was limited. Our results suggest that plural breeding results in greater fitness to mothers than solitary and singular breeding.

Onset of plural cooperative breeding in common marmoset families following replacement of the breeding male

Common marmosets, Callithrix jacchus, are usually characterized as singular cooperative breeders, with only a single, dominant female reproducing in each group. Anecdotal reports, however, have described two females breeding concurrently when an unrelated male joins their group. We tested the hypothesis that incorporation of an unrelated adult male into a family systematically leads to the onset of reproductive activity in a daughter and investigated the underlying mechanisms. We collected hormonal and behavioural data from mothers and their eldest daughters before and after the father was removed from the family and either replaced by an unrelated male ( N=11) or immediately returned to the family ( N=7). Variation between daughters in the occurrence of ovulatory cyclicity was not associated with the presence of an unrelated male but was closely linked to daughters' relationships with their mothers: only anovulatory daughters behaved submissively towards their mothers. Daughters never engaged in sexual behaviour with their fathers, but most did so with unrelated males. Similarly, daughters never conceived in intact natal families but did so in eight of 11 families containing an unrelated male. In six of these families, the mother and daughter bred concurrently. Thus, incorporation of an unrelated adult male into a marmoset family may frequently lead to the onset of plural breeding by activating sexual behaviour in a daughter; however, daughters ovulate only if they are not behaviourally subordinate to their mothers. Therefore, both inbreeding avoidance and rank-related reproductive suppression may constrain reproduction in marmoset daughters and contribute to maintenance of singular breeding.

Onset of plural cooperative breeding in common marmoset families following replacement of the breeding male

Common marmosets, Callithrix jacchus , are usually characterized as singular cooperative breeders, with only a single, dominant female reproducing in each group. Anecdotal reports, however, have described two females breeding concurrently when an unrelated male joins their group. We tested the hypothesis that incorporation of an unrelated adult male into a family systematically leads to the onset of reproductive activity in a daughter and investigated the underlying mechanisms. We collected hormonal and behavioural data from mothers and their eldest daughters before and after the father was removed from the family and either replaced by an unrelated male ( N =11) or immediately returned to the family ( N =7). Variation between daughters in the occurrence of ovulatory cyclicity was not associated with the presence of an unrelated male but was closely linked to daughters' relationships with their mothers: only anovulatory daughters behaved submissively towards their mothers. Daughters never engaged in sexual behaviour with their fathers, but most did so with unrelated males. Similarly, daughters never conceived in intact natal families but did so in eight of 11 families containing an unrelated male. In six of these families, the mother and daughter bred concurrently. Thus, incorporation of an unrelated adult male into a marmoset family may frequently lead to the onset of plural breeding by activating sexual behaviour in a daughter; however, daughters ovulate only if they are not behaviourally subordinate to their mothers. Therefore, both inbreeding avoidance and rank-related reproductive suppression may constrain reproduction in marmoset daughters and contribute to maintenance of singular breeding.

Phylogeny of Social Behavior in Aphelocoma Jays: A Role for Hybridization?

-The phylogeny of jays in the genus Aphelocoma describes the evolutionary appearance or disappearance of helping and other social behaviors that have been much studied in this genus. Using published allozyme data and new behavioral characters we reexamine the phylogeny of Aphelocoma. The best-fitting hypothesis is that the complex social system of the Mexican Jay (Aphelocoma ultramarina), including delayed maturation, helping, plural breeding, and loss of the rattle call, arose from a simpler state in a jay ancestor, perhaps one that already had occasional nonbreeding associates. The interpretation of phylogeny in eastern populations of the Mexican Jay may be complicated by hybridization with the Scrub Jay (A. coerulescens), suggesting the possibility of reticulate evolution in the genus. The Florida Scrub Jay (A. c. coerulescens) appears to be closely related to the population of Scrub Jays in southern Mexico, and together the two constitute a distinct clade within the Scrub Jay superspecies. Received 4 March 1994, accepted 28 January 1995. ALTHOUGH BEHAVIOR was used as a tool to study phylogeny in birds in the 1940s and 1950s (e.g. Lorenz 1941), the tables have turned recently; now phylogeny has become a tool to study the evolution of behavior (Brooks and McLennan 1991, Harvey and Pagel 1991, Harvey and Purvis 1991, Price 1991, Lanyon 1992, Richman and Price 1992). The evolution of social behavior in general and of helping behavior in particular can be studied in this way (Edwards and Naeem 1993). The genus Aphelocoma is a promising subject for such research because it spans the gamut from a complex, pluralbreeding system in the Mexican Jay (Aphelocoma ultramarina; Brown 1963), through a polyandrous system in the Unicolored Jay (A. unicolor; Webber and Brown 1994), to singular breeding in pairs with or without nonbreeding helpers in the Scrub Jay (A. coerulescens; Woolfenden 1975, Carmen 1989). The genus inhabits a wide range of habitats including Central American cloud forests (A. unicolor), pine-oak-juniper woodlands (A. ultramarina), and scrub vegetation (A. coerulescens). Some of the behavioral, phylogenetic, and taxonomic problems in this genus concern the populations of A. ultramarina that inhabit the Sierra Madre Oriental of eastern Mexico. This chain of montane populations includes two subspecies and extends from the Mexican state of Hidalgo (A. u. potosina) north to the Chisos Mountains on the Texas border (A. u. couchii). The Mexican Jay has two other groups of subspecies, a series of populations mainly in the mountains of western Mexico ranging from Arizona and New Mexico south through the Sierra Madre Occidental to Jalisco (arizonae, wollweberi, gracilis), and the populations crossing central Mexico in the Transvolcanic region (A. u. ultramarina, A. u. colimae). We refer to these geographic groups of subspecies as Orientalis, Occidentalis and Transvolcanic, respectively (Fig. 1). In this paper we survey the genus Aphelocoma with special reference to Orientalis. The Orientalis group may have been critical in the origin or loss of helping behavior in the genus (Brown and Horvath 1989, Peterson 1992b). Orientalis also has attracted the attention of behavioral ecologists because of the presence of certain Scrub-Jay-like behaviors and developmental patterns that are absent or weakly developed in other populations of the Mexican Jay. Three decades ago it was noticed that couchii, the population of Aphelocoma ultramarina in the border mountains of Texas and Coahuila, was in many respects somewhat intermediate between the Occidentalis group and the Scrub Jay (Brown 1963). Later, Orientalis was found to resemble the Scrub Jay in additional aspects of its social behavior (Brown and Horvath 1989). Northern populations of Orientalis possess a rattle call that is not found in the other groups (Strahl and Brown 1987 and earlier authors). In addition, sizes of territorial flocks in these populations are smaller, and the flocks appear to have only one breeding female each (singular

Plural Breeding in the Splendid Fairy‐wren, Malurus splendens (Aves: Maluridae), a Cooperative Breeder

AbstractGroups of the cooperatively breeding splendid fairy‐wren Malurus splendens may include more than one female. Previously this species has been described as singular breeding (only one female breeds). This paper describes the occurrence of plural breeding (PB) groups in 10% of group years, in which two females had separate nests. In all cases, the secondary female (Y) was related to the primary breeding female (X) and was generally a 2‐year old female which had helped in the group during the previous breeding season. Plural breeding was correlated with an increase in population density and in the number of female helpers; PB groups were larger than singular‐breeding groups. In most cases, the X female was occupied with her own nest or offspring when the Y female began to nest, and there was no aggression between them. Which birds helped the Y female to feed at her nest depended on the time between the hatching of the two nests. If the interval was small, some group members helped at each nest; with longer intervals, the group members began to feed at the earlier nest, and the other female was left to raise her brood alone. Female helpers were very active in feeding at single nestings, and the cost to an X female of a Y female breeding was mainly a loss of this assistance. The success of individual X nests was not affected. Effects on productivity were slight, but fewer X females in PB groups raised second broods than did experienced singular breeding females. Y females were less productive than X females, but no less productive than singular breeding novice females without helpers. It is not known whether Y females copulated with primary or secondary males within their group, or with males from outside the group. Certainly, they did not form an observable pairing with any male in the group. Plural breeding occurred in a minority of group years in response to extrinsic conditions and the current demographic situation, and shows the extreme plasticity of the mating system in M. splendens.

Geographic Variation of Group Size, Ontogeny, Rattle Calls, and Body Size in Aphelocoma ultramarina

Geographic Variation of Group Size, Ontogeny, Rattle Calls, and Body Size in Aphelocoma ultramarina

Parental facilitation: parent-offspring relations in communally breeding birds

A view of parent-offspring relations is developed that stresses an increased role for mutualism and tolerance rather than conflict in evolutionary trends toward sociality. For example, in Aphelocoma jays, parental tolerance of offspring increases from asocial to social species, contrary to what parental manipulation or parent-offspring conflict models have suggested. A simple model is presented in which parents can leave more grand-offspring while having fewer offspring through a mutualistic relationship between parent and offspring. Consistent with the model are the following observations: (1) At the extreme of sociality, in Mexican jays, A. ultramarina, both sexes commonly inherit their natal territory, thus retaining productive territories largely under control of genotypes that tolerate persistence of young in the territory. Sons and daughters may breed on their natal territory in the presence of their mothers and presumed fathers. (2) Jays banded as nestlings in the study area achieved higher reproductive success when breeding on their natal territory than those that moved to other territories. It is hypothesized that plural breeding can evolve as an extension of the trend leading to singular breeding via a non-altruistic reduction in the number of offspring per parent. The concept of parental facilitation may prove to be important for many highly social types of animals, including insects, birds and mammals.