Chromosome interaction over a distance in meiosis

Brady, Mary S.; Paliulis, Leocadia V.

doi:10.1098/rsos.150029

Cited by 9 publications

(8 citation statements)

References 36 publications

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“…We hypothesize that two of the 12 structures are X-and Y-chromosome univalents. This pattern of unpaired X and Y chromosomes at metaphase I is known among plant and insect species 48 . Korablev et al 47 observed that the X and Y pair end-to-end at metaphase I in Polydora curiosa, which therefore differs from S. benedicti.…”

Section: Karyotypingmentioning

confidence: 75%

Decoupled Maternal and Zygotic Genetic Effects Shape the Evolution of Development

Zakas

Deutscher

Kay

et al. 2017

Preprint

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Many animals develop indirectly via a larval stage that is morphologically and ecologically distinct from its adult form. Hundreds of lineages across animal phylogeny have secondarily lost larval forms, instead producing offspring that directly develop into adult form without a distinct larval ecological niche 1-7 . Indirect development in the sea is typically planktotrophic: females produce large numbers of small offspring that require exogenous planktonic food to develop before metamorphosing into benthic juveniles. Direct development is typically lecithotrophic: females produce a smaller number of larger eggs, each developing into a juvenile without the need for larval feeding, provisioned by yolk. Evolutionary theory suggests that these alternative developmental strategies represent stable alternative fitness peaks, while intermediate states are disfavored 4,8-11 . Transitions from planktotrophy to lecithotrophy thus require crossing a fitness valley and represent radical and coordinated transformations of life-history, fecundity, ecology, dispersal, and development 7,12-16 . Here we dissect this transition in Streblospio benedicti, the sole genetically tractable species that harbors both states as heritable variation [17][18][19] . We identify large-effect loci that act maternally to influence larval size and independent, unlinked large-effect loci that act zygotically to affect discrete aspects of larval morphology. Because lecithotrophs and planktotrophs differ in both size and morphology, the genetic basis of larval form exhibits strong maternal-by-zygotic epistasis for fitness 20 . The fitness of zygotic alleles depends on their maternal background, creating a positive frequency-dependence that may homogenize local populations. Developmental and population genetics interact to shape larval evolution.Streblospio benedicti females fall into two classes exhibiting classic life-history tradeoffs: Planktotrophic mothers produce small (~100um) eggs that develop into obligately feeding larvae that spend weeks in the plankton. These larvae are pelagic and grow larva-specific swimming chaetae that are thought to deter predation 21 (Fig 1a). Lecithotrophic mothers produce large (~200um) eggs that develop into larvae that do not require exogenous food and quickly leave the water column as benthic juveniles. These larvae lack swimming chaetae and a second type of larva-specific morphological structure, anal cirri containing bacillary cells, which are distinctive rhabdomeric cells of unknown function 22 (Fig 1a). There are also differences during embryogenesis 23 and organogenesis 22,24 , where accelerated development of juvenile features and truncated development of larval features occurs in lecithotrophs . Despite these developmental and larval differences, adults are indistinguishable at the level of gross morphology. Unlike examples of polyphenism, environmental input does not substantially alter egg size or subsequent offspring type 25,26 . S. benedicti is common throughout North American estuaries, but local p...

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Section: Karyotypingmentioning

confidence: 75%

Decoupled Maternal and Zygotic Genetic Effects Shape the Evolution of Development

Zakas

Deutscher

Kay

et al. 2017

Preprint

View full text Add to dashboard Cite

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“…We hypothesize that two of the 12 structures are X- and Y-chromosome univalents. This pattern of unpaired X and Y chromosomes at metaphase I is known among plant and insect species ( Brady and Paliulis, 2015 ). Korablev et al (1999) observed that the X and Y pair end-to-end at metaphase I in Polydora curiosa , which therefore differs from S. benedicti .…”

Section: Methodsmentioning

confidence: 85%

Decoupled maternal and zygotic genetic effects shape the evolution of development

Zakas

Deutscher

Kay

et al. 2018

eLife

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Evolutionary transitions from indirect to direct development involve changes in both maternal and zygotic genetic factors, with distinctive population-genetic implications, but empirical data on the genetics of such transitions are lacking. The polychaete Streblospio benedicti provides an opportunity to dissect a major transition in developmental mode using forward genetics. Females in this species produce either small eggs that develop into planktonic larvae or large eggs that develop into benthic juveniles. We identify large-effect loci that act maternally to influence larval size and independent, unlinked large-effect loci that act zygotically to affect discrete aspects of larval morphology. The likely fitness of zygotic alleles depends on their maternal background, creating a positive frequency-dependence that may homogenize local populations. Developmental and population genetics interact to shape larval evolution.

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“…Non-random segregation was first observed between two chromosomes in spermatocytes of the mole cricket Gryllotalpa borealis by Payne in 1912, and later confirmed by Camenzind and Nicklas (1968). Since then it has been observed in a variety of species, such as liverworts (Lorbeer 1934), flea beetles (Wilson et al 2003) and sciarid flies (Metz et al 1926), as reviewed in Brady and Paliulis (2015). For example, in mealy bugs and Sciara, all male-derived autosomes go to one pole and all female-derived chromosomes go to the other pole (mealy bugs : Schrader 1921: Schrader , 1923Nur 1982.…”

Section: Introductionmentioning

confidence: 94%

Chromosomes selectively detach at one pole and quickly move towards the opposite pole when kinetochore microtubules are depolymerized in Mesostoma ehrenbergii spermatocytes

Fegaras

Forer

2018

Protoplasma

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In a typical cell division, chromosomes align at the metaphase plate before anaphase commences. This is not the case in Mesostoma spermatocytes. Throughout prometaphase, the three bivalents persistently oscillate towards and away from either pole, at average speeds of 5-6 μm/min, without ever aligning at a metaphase plate. In our experiments, nocodazole (NOC) was added to prometaphase spermatocytes to depolymerize the microtubules. Traditional theories state that microtubules are the producers of force in the spindle, either by tubulin depolymerizing at the kinetochore (PacMan) or at the pole (Flux). Accordingly, if microtubules are quickly depolymerized, the chromosomes should arrest at the metaphase plate and not move. However, in 57/59 cells, at least one chromosome moved to a pole after NOC treatment, and in 52 of these cells, all three bivalents moved to the same pole. Thus, the movements are not random to one pole or other. After treatment with NOC, chromosome movement followed a consistent pattern. Bivalents stretched out towards both poles, paused, detached at one pole, and then the detached kinetochores quickly moved towards the other pole, reaching initial speeds up to more than 200 μm/min, much greater than anything previously recorded in this cell. As the NOC concentration increased, the average speeds increased and the microtubules disappeared faster. As the kinetochores approached the pole, they slowed down and eventually stopped. Similar results were obtained with colcemid treatment. Confocal immunofluorescence microscopy confirms that microtubules are not associated with moving chromosomes. Thus, these rapid chromosome movements may be due to non-microtubule spindle components such as actin-myosin or the spindle matrix.

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Chromosome interaction over a distance in meiosis

Cited by 9 publications

References 36 publications

Decoupled Maternal and Zygotic Genetic Effects Shape the Evolution of Development

Decoupled Maternal and Zygotic Genetic Effects Shape the Evolution of Development

Decoupled maternal and zygotic genetic effects shape the evolution of development

Chromosomes selectively detach at one pole and quickly move towards the opposite pole when kinetochore microtubules are depolymerized in Mesostoma ehrenbergii spermatocytes

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