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1. Eusociality and the transition from biparental to alloparental care in termites

   https://doi.org/10.1111/1365-2435.14183  

   Chouvenc, Thomas ( September 2022 , Functional Ecology)

   In eusocial organisms, cooperative brood care within a colony represents a situation where the ancestral parental care duties have shifted away from the reproductive parent(s) towards their offspring. The shift to alloparental care was often instrumental in the initial emergence of eusociality, as it ultimately contributed to the establishment of the reproductive division of labour.

   Remarkably, eusocial taxa such as ants and termites, which still display an ancestral independent colony foundation phase, must go through an obligatory parental care period, as a temporary subsocial family unit. In termites specifically, an incipient colony inherently remains a woodroach family unit until alloparental care is established. Colony foundation success can then be limited by a series of factors that may include environmental, behavioural, symbiotic and physiological constraints.

   In this study, 450 incipient termite colonies (Coptotermes gestroi) were established to investigate the timing of physiological changes in founders during the transition from biparental to alloparental care. Results showed that the finite initial internal nutritional resources that alates carry during the dispersal flight are a primary limiting factor for successful colony establishment. TheCoptotermesqueen and king must rapidly establish (<150 days) their first cohort of offspring to reach alloparental care or simply run out of resources and die. Alates, therefore, carry just enough internal resources to produce the first few alloparents (< 15 workers) to prime the system towards colony ergonomic growth, with a definitive shift to solely reproductive functions.

   Eusocial insect primary reproductive traits were optimized for three successive functions within the life cycle of a colony: alate dispersal (sexual reproduction), colony foundation (parental care) and colony growth (increased egg production towards colony maturity). However, results suggest that trade‐offs involving these functions appear to primarily favour dispersal ones (quantity vs. quality of alates), as founder(s) carry minimal resources and have no room for parental care inefficiency and as they then fully rely on their alloparents for further reproductive output.

   The transition towards alloparental care during colony foundation of eusocial insects may, therefore, reflect on the initial evolutionary transition from ancestral subsociality to eusociality.

   Read the freePlain Language Summaryfor this article on the Journal blog.

    

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2. Decoupled evolution of mating biology and social structure in Acromyrmex leaf-cutting ants

   https://doi.org/10.1007/s00265-021-03113-1  

   Dahan, Romain A. ; Grove, Nathan K. ; Bollazzi, Martin ; Gerstner, Benjamin P. ; Rabeling, Christian ( December 2021 , Behavioral Ecology and Sociobiology)

   Insect societies vary greatly in their social structure, mating biology, and life history. Polygyny, the presence of multiple reproductive queens in a single colony, and polyandry, multiple mating by females, both increase the genetic variability in colonies of eusocial organisms, resulting in potential reproductive conflicts. The co-occurrence of polygyny and polyandry in a single species is rarely observed across eusocial insects, and these traits have been found to be negatively correlated in ants.Acromyrmexleaf-cutting ants are well-suited for investigating the evolution of complex mating strategies because both polygyny and polyandry co-occur in this genus. We used microsatellite markers and parentage inference in five South AmericanAcromyrmexspecies to study how different selective pressures influence the evolution of polygyny and polyandry. We show thatAcromyrmexspecies exhibit independent variation in mating biology and social structure, and polygyny and polyandry are not necessarily negatively correlated within genera. One species,Acromyrmex lobicornis, displays a significantly lower mating frequency compared to others, while another species,A. lundii, appears to have reverted to obligate monogyny. These variations appear to have a small impact on average intra-colonial relatedness, although the biological significance of such a small effect size is unclear. All species show significant reproductive skew between patrilines, but there was no significant difference in reproductive skew between any of the sampled species. We find that the evolution of social structure and mating biology appear to follow independent evolutionary trajectories in different species. Finally, we discuss the evolutionary implications that mating biology and social structure have on life history evolution inAcromyrmexleaf-cutting ants.

   Many species of eusocial insects have colonies with multiple queens (polygyny), or queens mating with multiple males (polyandry). Both behaviors generate potentially beneficial genetic diversity in ant colonies as well as reproductive conflict. The co-occurrence of both polygyny and polyandry in a single species is only known from few ant species. Leaf-cutting ants have both multi-queen colonies and multiply mated queens, providing a well-suited system for studying the co-evolutionary dynamics between mating behavior and genetic diversity in colonies of eusocial insects. We used microsatellite markers to infer the socio-reproductive behavior in five South American leaf-cutter ant species. We found that variation in genetic diversity in colonies was directly associated with the mating frequencies of queens, but not with the number of queens in a colony. We suggest that multi-queen nesting and mating frequency evolve independently of one another, indicating that behavioral and ecological factors other than genetic diversity contribute to the evolution of complex mating behaviors in leaf-cutting ants.

    

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3. The Makorin lep-2 and the lncRNA lep-5 regulate lin-28 to schedule sexual maturation of the C. elegans nervous system

   https://doi.org/10.7554/eLife.43660  

   Lawson, Hannah ; Vuong, Edward ; Miller, Renee M ; Kiontke, Karin ; Fitch, David HA ; Portman, Douglas S ( July 2019 , eLife)

   Most animals develop from juveniles, which cannot reproduce, to sexually mature adults. The most obvious signs of this transition are changes in body shape and size. However, changes also take place in the brain that enable the animals to adapt their behavior to the demands of adulthood. For example, fully fed adult male roundworms will leave a food source to search for mates, whereas juvenile males will continue feeding. The transition to sexual maturity needs to be carefully timed. Too early, and the animal risks compromising key stages of development. Too late, and the animal may be less competitive in the quest for reproductive success. Cues in the environment, such as the presence of food and mates, interact with timing mechanisms in the brain to trigger sexual maturity. But how these mechanisms work – in particular where and how an animal keeps track of its developmental stage – is not well understood. In the roundworm species Caenorhabditis elegans, waves of gene activity, known collectively as the heterochronic pathway, determine patterns of cell growth as animals mature. Through further studies of these worms, Lawson et al. now show that these waves also control the time at which neural circuits mature. In addition, the waves of activity occur inside the nervous system itself, rather than in a tissue that sends signals to the nervous system. Moreover, they occur independently inside many different neurons. Each neuron thus has its own molecular clock for keeping track of development. Several of the genes critical for developmental timekeeping in worms are also found in mammals, including two genes that help to control when puberty starts in humans. If one of these genes – called MKRN3 – does not work correctly, it can lead to a condition that causes individuals to go through puberty several years earlier than normal. Studying the mechanisms identified in roundworms may help us to better understand this disorder. More generally, future work that builds on the results presented by Lawson et al. will help to reveal how environmental cues and gene activity interact to control when we become adults. 

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4. Effects of selective breeding for high voluntary wheel‐running behavior on femoral nutrient canal size and abundance in house mice

   https://doi.org/10.1111/joa.12830  

   Schwartz, Nicole E. ; Patel, Biren A. ; Garland, Jr, Theodore ; Horner, Angela M. ( May 2018 , Journal of Anatomy)

   Bone modeling and remodeling are aerobic processes that entail relatively high oxygen demands. Long bones receive oxygenated blood from nutrient arteries, epiphyseal‐metaphyseal arteries, and periosteal arteries, with the nutrient artery supplying the bulk of total blood volume in mammals (~ 50–70%). Estimates of blood flow into these bones can be made from the dimensions of the nutrient canal, through which nutrient arteries pass. Unfortunately, measuring these canal dimensions non‐invasively (i.e. without physical sectioning) is difficult, and thus researchers have relied on more readily visible skeletal proxies. Specifically, the size of the nutrient artery has been estimated from dimensions (e.g. minimum diameters) of the periosteal (external) opening of the nutrient canal. This approach has also been utilized by some comparative morphologists and paleontologists, as the opening of a nutrient canal is present long after the vascular soft tissue has degenerated. The literature on nutrient arteries and canals is sparse, with most studies consisting of anatomical descriptions from surgical proceedings, and only a few investigating the links between nutrient canal morphology and physiology or behavior. The primary objective of this study was to evaluate femur nutrient canal morphology in mice with known physiological and behavioral differences; specifically, mice from an artificial selection experiment for high voluntary wheel‐running behavior. Mice from four replicate high runner (HR) lines are known to differ from four non‐selected control (C) lines in both locomotor and metabolic activity, withHRmice having increased voluntary wheel‐running behavior and maximal aerobic capacity (VO₂max) during forced treadmill exercise. Femora from adult mice (average age 7.5 months) of the 11th generation of this selection experiment were μCT‐scanned and three‐dimensional virtual reconstructions of nutrient canals were measured for minimum cross‐sectional area as a skeletal proxy of blood flow. Gross observations revealed that nutrient canals varied far more in number and shape than prior descriptions would indicate, regardless of sex or genetic background (i.e.HRvs. C lines). Canals adopted non‐linear shapes and paths as they traversed from the periosteal to endosteal borders through the cortex, occasionally even branching within the cortical bone. Additionally, mice from bothHRand C lines averaged more than four nutrient canals per femur, in contrast to the one to two nutrient canals described for femora from rats, pigs, and humans in prior literature. Mice fromHRlines had significantly larger total nutrient canal area than C lines, which was the result not of an increase in the number of nutrient canals, but rather an increase in their average cross‐section size. This study demonstrates that mice with an evolutionary history of increased locomotor activity and maximal aerobic metabolic rate have a concomitant increase in the size of their femoral nutrient canals. Although the primary determinant of nutrient canal size is currently not well understood, the present results bolster use of nutrient canal size as a skeletal indicator of aerobically supported levels of physical activity in comparative studies.

    

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5. Journal of muscle research and cell motility, focus on Extreme Physiology Extreme Tolerance to Hypoxia, Hypercapnia, and Pain in the Naked Mole-Rat

   https://doi.org/10.1007/s10974-022-09623-3  

   Park, Thomas J. ; Reznick, Jane ( July 2022 , Journal of Muscle Research and Cell Motility)

   Abstract Challenging environmental conditions can drive the evolution of extreme physiological traits. The naked mole-rat has evolved to survive and thrive in a low oxygen, high carbon dioxide environment that would be deadly to humans and most other mammals. The naked mole-rat’s lifestyle is unusual in that this species combines subterranean living and living in large, social groups of up to 300 + individuals. Many respiring animals in a closed environment can lead to depletion of oxygen (hypoxia) and accumulation of carbon dioxide (hypercapnia). Naked mole-rats display a variety of physiological traits that negate the adverse effects of living in this atmosphere. For hypoxia tolerance, naked mole-rats have a low resting metabolism, high affinity hemoglobin, intrinsic brain tolerance, the ability to use fructose for anaerobic glycolysis, and the ability to enter a low energy, suspended animation-like state. For hypercapnia tolerance, these animals have a mutation in a voltage gated sodium channel that effectively eliminates neuronal responses to tissue acidosis. In other mammals, acidosis from exposure to high concentrations of carbon dioxide induces pain and pulmonary edema. Understanding these mechanisms of extreme physiology is not only inherently interesting, but it may lead to biomedical breakthroughs in research on heart attacks, strokes, and pain pathologies. 

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