SAPling: a Scan-Add-Print barcoding database system to label and track asexual organisms

Thomas, Michael A.; Schötz, Eva-Maria

doi:10.1242/jeb.059048

Cited by 6 publications

(7 citation statements)

References 56 publications

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“…[36]. In recording the reproductive events of 15,030 S-, 6,229 J-and 2,492 G-worm, we obtained unprecedented statistical insight into the asexual reproductive strategies for each of the three planarian species.…”

Section: Resultsmentioning

confidence: 97%

“…Upon asexual reproduction, the reproductive event was recorded in the SAPling database as described in detail in Ref. [36]. Worm reproductive waiting times (RWTs) and the type of reproductive event (fission vs. fragmentation) were recorded as previously described in Ref.…”

Section: Isolated Worm Experimentsmentioning

confidence: 99%

“…Using such a large-scale, long-term experiment [36] tracking thousands of reproductive events, we have previously studied, both experimentally and theoretically, the life history strategy of S-planarians in great detail [12,25,37]. Statistical analysis of the reproductive behavior of individual worms in isolation revealed that S-planarians exhibit a randomized reproductive strategy with respect to the number of offspring produced per reproductive event.…”

Section: Introductionmentioning

confidence: 99%

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To Each His Own

et al. 2015

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Planarians are among the most complex animals with the ability to regenerate complete organisms from small tissue pieces. This ability allows them to reproduce by splitting themselves into a head and a tail piece, making them a rare example of asexual reproduction via transverse fission in multi-cellular organisms. Due to the stochastic nature of long reproductive cycles, which range from days to months, few and primarily qualitative studies have been conducted to understand the reproductive behaviors of asexual planarians. We have executed the largest long-term study on planarian asexual reproduction to date, tracking more than 23,000 reproductive events of three common planarian species found in Europe, North America, and Asia, respectively: Schmidtea mediterranea, Dugesia tigrina, and Dugesia japonica. This unique data collection allowed us to perform a detailed statistical analysis of their reproductive strategies. Since the three species share a similar anatomy and mode of reproduction by transverse division, we were surprised to find that each species had acquired its own distinct strategy for optimizing its reproductive success. We statistically examined each strategy, associated trade-offs, and the potential regulatory mechanisms on the population level. Interestingly, models for cell cycle length regulation in unicellular organisms could be directly applied to describe reproductive cycle lengths of planarians, despite the difference in underlying biological mechanisms. Finally, we exam-Electronic supplementary material The online version of this article (ined the ecological implications of each strategy through intra-and inter-species competition experiments and found that D. japonica outcompeted the other two species due to its relatively equal distribution of resources on head and tail pieces, its cannibalistic behaviors and ability to thrive in crowded environments. These results show that this species would pose a serious threat to endogenous planarian populations if accidentally introduced in their habitats.

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Section: Resultsmentioning

confidence: 97%

Section: Isolated Worm Experimentsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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et al. 2015

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“…Fissions were tracked using the SAPling database and barcode system (35) and planarian head and tail sizes were quantified as described in detail in the SI Materials and Methods.…”

Section: Methodsmentioning

confidence: 99%

Mechanics dictate where and how freshwater planarians fission

Malinowski

Cochet‐Escartin

Kaj

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Asexual freshwater planarians reproduce by tearing themselves into two pieces by a process called binary fission. The resulting head and tail pieces regenerate within about a week forming two new worms. Understanding this process of ripping oneself into two parts poses a challenging biomechanical problem. Since planarians stop "doing it" at the slightest disturbance, this remained a centuries-old puzzle. We focus on Dugesia japonica fission and show that it proceeds in three stages: a local constriction ("waist formation"), pulsationwhich increases waist longitudinal stresses -and transverse rupture. We developed a linear mechanical model with a planarian represented by a thin shell. The model fully captures the pulsation dynamics leading to rupture and reproduces empirical time scales and stresses. It asserts that fission execution is a mechanical process. Furthermore, we show that the location of waist formation, and thus fission, is determined by physical constraints. Together, our results demonstrate that where and how a planarian rips itself apart during asexual reproduction can be fully explained through biomechanics.Keywords: planarians, biomechanics, fission, rupture, traction forces Significance Statement: How planarians reproduce by ripping themselves into a head and a tail piece, which subsequently regenerate into two new worms, is a centuries-old biomechanics problem. Michael Faraday contemplated how this feat can be achieved in the 1800s, but it remained unanswered because it is experimentally difficult to observe planarians "doing it". We recorded Dugesia japonica planarians in the act and developed a physical model which captures pivotal steps of their reproduction dynamics. The model reproduces experimental time scales and rupture stresses without fit parameters. The key to rupture is a local reduction of the animal's cross-sectional area, which greatly amplifies the stresses exerted by the planarian's musculature and enables rupture at substrate stresses in the Pa range. \body Already Michael Faraday and his contemporaries were intrigued by the observation that asexual freshwater planarians, squishy worms a few mm in length, reproduced by tearing themselves into a head and tail offspring, in a process called binary fission (1). How was it possible for these animals to generate the forces necessary to rip themselves using only their

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“…a trunk fragment containing largely intestine must generate new positional information to specify head and tail regions). The incomplete reprogramming of these markers may lead to their maintenance throughout the complete animal ( Thomas and Schötz, 2011 ). In other words, an organism that regenerates from a tail may be more ‘tail-like’ than one that regenerates from a head.…”

Section: Suggested Experimentsmentioning

confidence: 99%

Vertically- and horizontally-transmitted memories – the fading boundaries between regeneration and inheritance in planaria

2016

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The Weismann barrier postulates that genetic information passes only from the germline to the soma and not in reverse, thus providing an obstacle to the inheritance of acquired traits. Certain organisms such as planaria – flatworms that can reproduce through asymmetric fission – avoid the limitations of this barrier, thus blurring the distinction between the processes of inheritance and development. In this paper, we re-evaluate canonical ideas about the interaction between developmental, genetic and evolutionary processes through the lens of planaria. Biased distribution of epigenetic effects in asymmetrically produced parts of a regenerating organism could increase variation and therefore affect the species' evolution. The maintenance and fixing of somatic experiences, encoded via stable biochemical or physiological states, may contribute to evolutionary processes in the absence of classically defined generations. We discuss different mechanisms that could induce asymmetry between the two organisms that eventually develop from the regenerating parts, including one particularly fascinating source – the potential capacity of the brain to produce long-lasting epigenetic changes.

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SAPling: a Scan-Add-Print barcoding database system to label and track asexual organisms

Cited by 6 publications

References 56 publications

To Each His Own

To Each His Own

Mechanics dictate where and how freshwater planarians fission

Vertically- and horizontally-transmitted memories – the fading boundaries between regeneration and inheritance in planaria

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