The Sperm/Oocyte Decision, a<i>C. elegans</i>Perspective

Ellis, Ronald

doi:10.1002/9780470687970.ch1

Cited by 5 publications

(6 citation statements)

References 121 publications

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“…). While it is possible that such genes directly regulate the central germline sex determination pathway, for example, fog‐2 (Schedl and Kimble ), additional genes may also act indirectly on germ cell proliferation and differentiation, through a variety of possible soma‐germline interactions, in particular, interactions mediated by the somatic gonad (Ellis ; Korta and Hubbard ). Whether regulatory changes in genes of the so‐called “heterochronic pathway,” whose mutational disruption causes pronounced temporal shifts in the progression of certain somatic C. elegans cell lineages (Resnick et al.…”

Section: Discussionmentioning

confidence: 99%

“…Transcriptomic analyses of the temporal dynamics of gene expression associated with germline versus somatic development provide many potential candidates (Thoemke et al 2005;Spencer et al 2011). While it is possible that such genes directly regulate the central germline sex determination pathway, for example, fog-2 (Schedl and Kimble 1988), additional genes may also act indirectly on germ cell proliferation and differentiation, through a variety of possible soma-germline interactions, in particular, interactions mediated by the somatic gonad (Ellis 2010;Korta and Hubbard 2010). Whether regulatory changes in genes of the so-called "heterochronic pathway," whose mutational disruption causes pronounced temporal shifts in the progression of certain somatic C. elegans cell lineages (Resnick et al 2010), could preferentially contribute to the evolution by heterochrony remains questionable, not only with respect to our experimental paradigm but in general.…”

Section: Discussionmentioning

confidence: 99%

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Complex heterochrony underlies the evolution ofCaenorhabditis eleganshermaphrodite sex allocation

et al. 2016

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Hermaphroditic organisms are key models in sex allocation research, yet the developmental processes by which hermaphrodite sex allocation can evolve remain largely unknown. Here we use experimental evolution of hermaphrodite-male (androdioecious) Caenorhabditis elegans populations to quantify the developmental changes underlying adaptive shifts in hermaphrodite sex allocation. We show that the experimental evolution of increased early-life self-fertility occurred through modification of a suite of developmental traits: increased self-sperm production, accelerated oogenesis and ovulation, and increased embryo retention. The experimental evolution of increased self-sperm production delayed entry into oogenesis-as expected, given the sequentially coupled production of self-spermatogenesis and oogenesis. Surprisingly, however, delayed oogenesis onset did not delay reproductive maturity, nor did it trade-off with gamete or embryo size. Comparing developmental time dynamics of germline and soma indicates that the evolution of increased sperm production did not delay reproductive maturity due to a globally accelerated larval development during the period of self-spermatogenesis. Overall, heterochrony in gametogenesis and soma can explain adaptive shifts in hermaphrodite sex allocation.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Complex heterochrony underlies the evolution ofCaenorhabditis eleganshermaphrodite sex allocation

et al. 2016

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“…In C. elegans, a population of mitotic precursors is maintained through proliferative signals emanating from the Distal Tip Cell, which defines the germ stem cell niche (Austin and Kimble 1987;Henderson et al 1994). As mitotic cells move proximally, they enter progressive steps of meiosis and initially differentiate into sperm during the last larval stage, then exclusively into oocytes for the remainder of adult life (Ellis 2010). Germ cell proliferation and oocyte differentiation are maintained throughout the reproductive period, with adult hermaphrodites containing approximately 1000 germ cells per gonad arm (Kimble and Crittenden 2007).…”

Section: Introductionmentioning

confidence: 99%

“…The three androdioecious Caenorhabditis species reproduce primarily through self-fertilizing hermaphrodites F elix 2005, 2007;Gimond et al 2013; Thomas et al 2015), and the basic organization of their gonad, consisting of two bilaterally symmetric arms, appear very similar (Rudel and Kimble 2001;Kimble and Crittenden 2007;Haag 2009;Ellis 2010;Thomas et al 2012) (Fig. 1A).…”

Section: Introductionmentioning

confidence: 99%

Evolutionarily divergent thermal sensitivity of germline development and fertility in hermaphroditic Caenorhabditis nematodes

Poullet

Vielle

Gimond

et al. 2015

Evolution and Development

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Thermal developmental plasticity represents a key organismal adaptation to maintain reproductive capacity in contrasting and fluctuating temperature niches. Although extensively studied, research on thermal plasticity has mainly focused on phenotypic outcomes, such as adult life history, rather than directly measuring plasticity of underlying developmental processes. How thermal plasticity of developmental phenotypes maps into plasticity of resulting final phenotypes, and how such mapping relationships evolve, thus remain poorly understood. Here we address these questions by quantifying thermal plasticity of Caenorhabditis hermaphrodite germline development. We integrate measurements of germline development and fertility at the upper thermal range in isolates of C. briggsae, C. elegans, and C. tropicalis. First, we compare intra- and interspecific variation in thermal germline plasticity with plasticity in reproductive output. Second, we ask whether the developmental errors leading to fertility break-down at upper thermal limits are evolutionarily conserved. We find that temperature variation modulates spermatogenesis, oogenesis and germ cell progenitor pools, yet the thermal sensitivity of these processes varies among isolates and species, consistent with evolutionary variation in upper thermal limits of hermaphrodite fertility. Although defective sperm function is a major contributor to heat-induced fertility break-down, high temperature also significantly perturbs oogenesis, germline integrity, and mitosis-meiosis progression. Remarkably, the occurrence and frequency of specific errors are strongly species- and genotype-dependent, indicative of evolutionary divergence in thermal sensitivity of distinct processes in germline development. Therefore, the Caenorhabditis reproductive system displays complex genotype-by-temperature interactions at the developmental level, which may remain masked when studying thermal plasticity exclusively at the life history level.

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“…In sum, gamete fate specification is the binary readout of a complex network composed of at least three regulatory inputs. Most regulatory relationships in Figure 7A are well established (see reviews by Zarkower 2006;Ellis and Schedl 2007;Kimble and Crittenden 2007;Ellis 2010;Sundaram 2013), but the MPK-1/ERK substrates for gamete specification and the full spectrum of PUF-8 and FBF-1 individual and joint target mRNAs remain unknown.…”

Section: A Model For Chemical Reprogramming and The Sperm/oocyte Regumentioning

confidence: 99%

Competence for Chemical Reprogramming of Sexual Fate Correlates with an Intersexual Molecular Signature inCaenorhabditis elegans

2014

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In multicellular organisms, genetic programs guide cells to adopt cell fates as tissues are formed during development, maintained in adults, and repaired after injury. Here we explore how a small molecule in the environment can switch a genetic program from one fate to another. Wild-type Caenorhabditis elegans XX adult hermaphrodites make oocytes continuously, but certain mutant XX adults make sperm instead in an otherwise hermaphrodite soma. Thus, puf-8; lip-1 XX adults make only sperm, but they can be switched from sperm to oocyte production by treatment with a small-molecule MEK inhibitor. To ask whether this chemical reprogramming is common, we tested six XX sperm-only mutants, but found only one other capable of cell fate switching, fbf-1; lip-1. Therefore, reprogramming competence relies on genotype, with only certain mutants capable of responding to the MEK inhibitor with a cell fate change. To gain insight into the molecular basis of competence for chemical reprogramming, we compared polyadenylated transcriptomes of competent and noncompetent XX sperm-only mutants in the absence of the MEK inhibitor and hence in the absence of cell fate reprogramming. Despite their cellular production of sperm, competent mutants were enriched for oogenic messenger RNAs relative to mutants lacking competence for chemical reprogramming. In addition, competent mutants expressed the oocyte-specific protein RME-2, whereas those lacking competence did not. Therefore, mutants competent for reprogramming possess an intersexual molecular profile at both RNA and protein levels. We suggest that this intersexual molecular signature is diagnostic of an intermediate network state that poises the germline tissue for changing its cellular fate in response to environmental cues. C ELLS in multicellular organisms acquire specific fates, either during development as tissues are generated or during adulthood as tissues are renewed or repaired. A classical view holds that during development, a cell follows a specific genetic program to determine its differentiated fate, but more recent studies reveal that cells can be induced to switch from one genetic program to another. Such "reprogramming" of a cell fate program can occur in vivo in cancer (Friedl and Alexander 2011;Byun and Gardner 2013), wound healing (Wong et al. 2013), and regeneration (Xin et al. 2013;Ziv et al. 2013). Moreover, reprogramming can be stimulated by introduction of transcription factors (Takahashi and Yamanaka 2006) or small molecules (Morgan et al. 2010;Zhu et al. 2010;Li et al. 2014). Here we explore the effect of genotype on the capacity for a particular case of chemically induced cell fate reprogramming within an organism.The Caenorhabditis elegans germline provides a tractable model for analyses of cell fate reprogramming. The adult germline is an elongate tissue with 2000 cells, including germline stem cells (GSCs) (Figure 1A, yellow). GSCs continuously generate daughter cells that enter the meiotic cell cycle ( Figure 1A, green) and then differentiate as...

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The Sperm/Oocyte Decision, aC. elegansPerspective

Cited by 5 publications

References 121 publications

Complex heterochrony underlies the evolution ofCaenorhabditis eleganshermaphrodite sex allocation

Complex heterochrony underlies the evolution ofCaenorhabditis eleganshermaphrodite sex allocation

Evolutionarily divergent thermal sensitivity of germline development and fertility in hermaphroditic Caenorhabditis nematodes

Competence for Chemical Reprogramming of Sexual Fate Correlates with an Intersexual Molecular Signature inCaenorhabditis elegans

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