Coordination Between the Sexes Constrains the Optimization of Reproductive Timing in Honey Bee Colonies.
ABSTRACT: Honeybees are an excellent model system for examining how trade-offs shape reproductive timing in organisms with seasonal environments. Honeybee colonies reproduce two ways: producing swarms comprising a queen and thousands of workers or producing males (drones). There is an energetic trade-off between producing workers, which contribute to colony growth, and drones, which contribute only to reproduction. The timing of drone production therefore determines both the drones' likelihood of mating and when colonies reach sufficient size to swarm. Using a linear programming model, we ask when a colony should produce drones and swarms to maximize reproductive success. We find the optimal behavior for each colony is to produce all drones prior to swarming, an impossible solution on a population scale because queens and drones would never co-occur. Reproductive timing is therefore not solely determined by energetic trade-offs but by the game theoretic problem of coordinating the production of reproductives among colonies.
Project description:Eusociality, one of the most complex forms of social organization, is thought to have evolved in several animal clades in response to competition for resources and reproductive opportunities. Several species of snapping shrimp in the genus Synalpheus, the only marine organisms known to exhibit eusociality, form colonies characterized by high reproductive skew, and aggressive territoriality coupled with cooperative defense. In eusocial Synalpheus colonies, individual reproduction is limited to female 'queens', whose fecundity dictates colony growth. Given that individual reproduction and defense are both energetically costly, individual and colony fitness likely depend on the optimal allocation of resources by these reproducing individuals towards these potentially competing demands. Synalpheus species, however, display varying degrees of eusociality, suggesting that reproducing females have adopted different strategies for allocation among reproduction and defense. Here, we use structural equation modeling to characterize the relationships between the allometry of queen reproductive capacity and defensive weaponry, and colony size in six eusocial Synalpheus species, estimating trade-offs between reproduction and defense. We document strong trade-offs between mass of the fighting claw (defense) and egg number (reproduction) in queens from weakly eusocial species, while the trade-off is reduced or absent in those from strongly eusocial species. These results suggest that in less cooperative species, intra-colony conflict selects for queen retention of weapons that have significant costs to fecundity, while reproducing females from highly eusocial species, i.e., those with a single queen, have been able to reduce the cost of weapons as a result of protection by other colony members.
Project description:As yet, certain aspects of the Africanization process are not well understood, for example, the reproductive behavior of African and European honeybees and how the first Africanized swarms were formed and spread. Drone congregation areas (DCAs) are the ideal place to study honeybee reproduction under natural conditions since hundreds of drones from various colonies gather together in the same geographical area for mating. In the present study, we assessed the genetic structure of seven drone congregations and four commercial European-derived and Africanized apiaries in southern Brazil, employing seven microsatellite loci for this purpose. We also estimated the number of mother-colonies that drones of a specific DCA originated from. Pairwise comparison failed to reveal any population sub-structuring among the DCAs, thus indicating low mutual genetic differentiation. We also observed high genetic similarity between colonies of commercial apiaries and DCAs, besides a slight contribution from a European-derived apiary to a DCA formed nearby. Africanized DCAs seem to have a somewhat different genetic structure when compared to the European.
Project description:Honey bee (Apis mellifera) colonies invest a substantial amount of colony resources in the production of drones during the reproductive season to enable mating with virgin queens from nearby colonies. Recent studies have shown significant differences in the production of sperm cells that are viable (i.e., sperm viability) and can fertilize an ovule among sexually mature drones that are exposed to different environmental conditions during development or as adults. In particular, sperm viability may be negatively affected during drone development from exposure to pesticides in contaminated beeswax. To assess whether sperm viability is negatively affected during drone development from exposure to beeswax contaminated with in-hive pesticides, we compared the viability of sperm collected from drones reared in pesticide-free beeswax with that of drones reared in beeswax contaminated with field-relevant concentrations of the pesticides most commonly found in wax from commercial beekeeping operations in the United States. These pesticides include the miticides fluvalinate, coumaphos and amitraz, and the agro-chemicals chlorothalonil and chlorpyrifos. Sperm from drones collected at 10 and 18 days post emergence were classified as viable or non-viable to calculate sperm viability. For all pesticide treatment groups, drones that were reared in pesticide-laden beeswax had lower sperm viability compared to those reared in pesticide-free beeswax. This difference was especially pronounced among drones reared in miticide-laden wax. Our results reinforce the notion that pesticide contamination of beeswax negatively affects the reproductive quality of drones, which can affect the queens they mate with, ultimately compromising colony health.
Project description:The giant honeybee Apis dorsata often forms dense colony aggregations which can include up to 200 often closely related nests in the same location, setting the stage for inbred matings. Yet, like in all other Apis species, A. dorsata queens mate in mid-air on lek like drone congregation areas (DCAs) where large numbers of males gather in flight. We here report how the drone composition of A. dorsata DCAs facilitates outbreeding, taking into the account both spatial (three DCAs) and temporal (subsequent sampling days) dynamics. We compared the drones' genotypes at ten microsatellite DNA markers with those of the queen genotypes of six drone-producing colonies located close to the DCAs (Tenom, Sabah, Malaysia). None of 430 sampled drones originated from any of these nearby colonies. Moreover, we estimated that 141 unidentified colonies were contributing to the three DCAs. Most of these colonies were participating multiple times in the different locations and/or during the consecutive days of sampling. The drones sampled in the DCAs could be attributed to six subpopulations. These were all admixed in all DCA samples, increasing the effective population size an order of magnitude and preventing matings between potentially related queens and drones.
Project description:The question on how individuals allocate resources into maintenance and reproduction is one of the central questions in life history theory. Yet, resource allocation into maintenance on the organismic level can only be measured indirectly. This is different in a social insect colony, a "superorganism" where workers represent the soma and the queen the germ line of the colony. Here, we investigate whether trade-offs exist between maintenance and reproduction on two levels of biological organization, queens and colonies, by following single-queen colonies of the ant Cardiocondyla obscurior throughout the entire lifespan of the queen. Our results show that maintenance and reproduction are positively correlated on the colony level, and we confirm results of an earlier study that found no trade-off on the individual (queen) level. We attribute this unexpected outcome to the existence of a positive feedback loop where investment into maintenance (workers) increases the rate of resource acquisition under laboratory conditions. Even though food was provided ad libitum, variation in productivity among the colonies suggests that resources can only be utilized and invested into additional maintenance and reproduction by the colony if enough workers are available. The resulting relationship between per-capita and colony productivity in our study fits well with other studies conducted in the field, where decreasing per-capita productivity and the leveling off of colony productivity have been linked to density dependent effects due to competition among colonies. This suggests that the absence of trade-offs in our laboratory study might also be prevalent under natural conditions, leading to a positive association of maintenance, (= growth) and reproduction. In this respect, insect colonies resemble indeterminate growing organisms.
Project description:Social insect colonies can be seen as a distinct form of biological organisation because they function as superorganisms. Understanding how natural selection acts on the emergence and maintenance of these colonies remains a major question in evolutionary biology and ecology. Here, we explore this by using multi-type branching processes to calculate the basic reproductive ratios and the extinction probabilities for solitary vs. eusocial reproductive strategies. We find that eusociality, albeit being hugely successful once established, is generally less stable than solitary reproduction unless large demographic advantages of eusociality arise for small colony sizes. We also demonstrate how such demographic constraints can be overcome by the presence of ecological niches that strongly favour eusociality. Our results characterise the risk-return trade-offs between solitary and eusocial reproduction, and help to explain why eusociality is taxonomically rare: eusociality is a high-risk, high-reward strategy, whereas solitary reproduction is more conservative.
Project description:Sexually selected weapons are assumed to trade off with traits related to ejaculates, such as testes. However, remarkably little is known about what governs resource allocation and why trade-offs are found in some cases and not others. Often-used models depict competitive allocation occurring within the functional grouping of traits (e.g. reproduction); however, other factors including tissue expense and developmental timing may influence allocation. Experimental comparisons of investment across the sexes have the potential to illuminate allocation rules, because the sexes do not always use traits for the same functions. Here, we capitalize upon a species where females have weapons-testes homologues. We report that a documented trade-off in investment between hind-limb weapons and testes in leaf-footed cactus bugs, Narnia femorata, is even more pronounced in female hind limbs and ovaries. Female hind limbs in this species do not share the clear reproductive function of male hind limbs; therefore, this trade-off spans trait functional groups. Such patterns of investment suggest that future studies of reproductive trade-offs should consider factors such as tissue expense and developmental timing.
Project description:The patterned way in which individuals allocate finite resources to various components of reproduction (e.g. mating effort, reproductive timing and parental investment) is described as a reproductive strategy. As energy is limited, trade-offs between and within aspects of reproductive strategies are expected. The first aim of this study was to derive aspects of reproductive strategies using complete reproductive histories from 718 parous Western Australian women. Factor analysis using a subset of these participants resulted in six factors that represented 'short-term mating strategy', 'early onset of sexual activity', 'reproductive output', 'timing of childbearing', 'breastfeeding', and 'child spacing'. This factor structure was internally validated by replication using a second independent subset of the data. The second aim of this study examined trade-offs between aspects of reproductive strategies derived from aim one. Factor scores calculated for each woman were incorporated in generalised linear models and interaction terms were employed to examine the effect of mating behaviour on the relationships between reproductive timing, parental investment and overall reproductive success. Early sexual activity correlates with early reproductive onset for women displaying more long-term mating strategies. Women with more short-term mating strategies exhibit a trade-off between child quantity and child quality not observed in women with a long-term mating strategy. However, women with a short-term mating strategy who delay reproductive timing exhibit levels of parental investment (measured as breastfeeding duration per child) similar to that of women with long-term mating strategies. Reproductive delay has fitness costs (fewer births) for women displaying more short-term mating strategies. We provide empirical evidence that reproductive histories of contemporary women reflect aspects of reproductive strategies, and associations between these strategic elements, as predicted from life history theory.
Project description:OBJECTIVE:Life-history strategies promote reproductive fitness and survival. Limited energy availability and competing energetic demands between life-history decisions may result in organismal trade-offs leading to selection for "optimal" traits that facilitate fitness and survival in present environmental conditions. Few life-history analyses have been conducted in food abundant/high resource human populations. Here, we use a life-history theory framework integrated with a biocultural approach to assess whether trade-offs between growth (height) and the onset of reproductive maturation (ages at menarche) were observed in a sample of adult women living in the United States. METHODS:Adult women (18?years and older) from the National Health and Nutrition Examination Survey (NHANES) 2005 to 2006 were analyzed using complex survey regression to evaluate associations between ages at menarche, height, and biological, socio-economic, demographic, and anthropometric variables. Associations between stature, ages at menarche, and socio-economic status (household income and education level) suggest life-history trade-offs in this populations may be mitigated by access to resources and marginalization. CONCLUSIONS:These study results have applied public health implications. We demonstrate that females who experience early menarche in the US population achieve short stature. Our study also demonstrates the need for implementing life-history analyses in Western affluent populations, where marginalization may result in life-history trade-offs.
Project description:Plant reproductive trade-offs are thought to be caused by resource limitations or other constraints, but more empirical support for these hypotheses would be welcome. Additionally, quantitative characterization of these trade-offs, as well as consideration of whether they are linear, could yield additional insights. We expanded our flower removal research on lowbush blueberry (Vaccinium angustifolium) to explore the nature of and causes of its reproductive trade-offs. We used fertilization, defoliation, positionally biased flower removal, and multiple flower removal levels to discern why reproductive trade-offs occur in this taxon and to plot these trade-offs along two continuous axes. We found evidence through defoliation that vegetative mass per stem may trade off with reproductive effort in lowbush blueberry because the two traits compete for limited carbon. Also, several traits including ripe fruit production per reproductive node and fruit titratable acidity may be "sink-limited"-they decline with increasing reproductive effort because average reproductive structure quality declines. We found no evidence that reproductive trade-offs were caused by nitrogen limitation. Use of reproductive nodes remaining per stem as a measure of reproductive effort indicated steeper trade-offs than use of the proportion of nodes remaining. For five of six traits, we found evidence that the trade-off could be concave down or up instead of strictly linear. Synthesis. To date, studies have aimed primarily at identifying plant reproductive trade-offs. However, understanding how and why these trade-offs occur represent the exciting and necessary next steps for this line of inquiry.