Limits...
Desiccation plasticity in the embryonic life histories of non-annual rivulid species.

Varela-Lasheras I, Van Dooren TJ - Evodevo (2014)

Bottom Line: We have estimated effects on developmental and mortality rates during and after the desiccation treatment.Embryos of these non-annual rivulids decreased their developmental rates in early stages of development in response to desiccation and this effect persisted after the treatment.In one of these, we found cohorts of embryos in the latest stages of development that did not hatch over a period of more than 1 month without mortality.

View Article: PubMed Central - HTML - PubMed

Affiliation: Naturalis Biodiversity Center, Darwinweg 2, Leiden 2333 CR, The Netherlands ; Current address: Instituto Gulbenkian de Ciência, Rua da Quinta Grande 6, 2780-156 Oeiras, Portugal.

ABSTRACT

Background: Diapause is a developmental arrest present in annual killifish, whose eggs are able to survive long periods of desiccation when the temporary ponds they inhabit dry up. Diapause can occur in three different developmental stages. These differ, within and between species, in their responsiveness to different environmental cues. A role of developmental plasticity and genetic assimilation in diapause evolution has been previously suggested but not experimentally explored. We investigated whether plastic developmental delays or arrests provoked by an unusual and extreme environment could be the ancestral condition for diapause. This would be in agreement with plasticity evolution playing a role in the emergence of diapause in this group. We have used a comparative experimental approach and exposed embryos of non-annual killifish belonging to five different species from the former genus Rivulus to brief periods of desiccation. We have estimated effects on developmental and mortality rates during and after the desiccation treatment.

Results: Embryos of these non-annual rivulids decreased their developmental rates in early stages of development in response to desiccation and this effect persisted after the treatment. Two pairs of two different species had sufficient sample sizes to investigate rates of development in later stages well. In one of these, we found cohorts of embryos in the latest stages of development that did not hatch over a period of more than 1 month without mortality. Several properties of this arrest are also used to characterize diapause III in annual killifish. Such a cohort is present in control conditions and increases in frequency in the desiccation treatment.

Conclusions: The presence of plasticity for developmental timing and a prolonged developmental arrest in non-annual rivulids, suggest that a plastic developmental delay or diapause might have been present in the shared ancestor of annual and non-annual South American killifish and that the evolution of plasticity could have played a role in the emergence of the diapauses. Further comparative experimental studies and field research are needed to better understand how diapause and its plasticity evolved in this group.

No MeSH data available.


Related in: MedlinePlus

Upper row: developmental stages in Rivulus spp. (A) Stage one: approximately 50% epiboly; (B) Stage two: neural keel. (C) Stage three: optic cups; (D) Stage four: pigmentation in eyes and skin; (E) Stage five: embryo surrounding yolk sac. Lower row: (F-I) Morphological effects of air-exposed development. (A, B, F, G)C. magdalenae. (C, H, I)C. brunneus. (D)L. frenatus. (E)C. kuelpmannii. Images are not to scale.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
getmorefigures.php?uid=PMC4016651&req=5

Figure 1: Upper row: developmental stages in Rivulus spp. (A) Stage one: approximately 50% epiboly; (B) Stage two: neural keel. (C) Stage three: optic cups; (D) Stage four: pigmentation in eyes and skin; (E) Stage five: embryo surrounding yolk sac. Lower row: (F-I) Morphological effects of air-exposed development. (A, B, F, G)C. magdalenae. (C, H, I)C. brunneus. (D)L. frenatus. (E)C. kuelpmannii. Images are not to scale.

Mentions: We collected 209 eggs from C. brunneus, 112 from C. magdalenae, 23 from C. kuelpmanni, 11 from A. immaculatus, and 10 eggs from L. frenatus (all 10 in the test group). Numbers of embryos that reached each developmental stage and numbers hatched are given per pair and per treatment in Table 1. The overall median time duration of the desiccation treatment among the embryos that were returned to water was 8 days (eight for C. brunneus, six for C. magdalenae). Effects of developing in air were visible few hours after the start of the treatment. Generally, after 48 hours egg envelopes became opaque and rough, depressions in the egg surface appeared and eggs started shrinking (Figure 1). However, these effects were variable in different embryos (see Figure 1I and H for embryos from the same clutch experiencing identical conditions). Few embryos were returned from the desiccation treatment into water before they reached stage three. Therefore, assuming a potential lack of power, we did not expect any significant period effects and effects of the duration of the dry period experienced for stages one and two. In none of the analysis, rates in the Test and Control groups were different and we pooled these groups for the presentation of results. We therefore only present Control and Desiccation treatment levels.


Desiccation plasticity in the embryonic life histories of non-annual rivulid species.

Varela-Lasheras I, Van Dooren TJ - Evodevo (2014)

Upper row: developmental stages in Rivulus spp. (A) Stage one: approximately 50% epiboly; (B) Stage two: neural keel. (C) Stage three: optic cups; (D) Stage four: pigmentation in eyes and skin; (E) Stage five: embryo surrounding yolk sac. Lower row: (F-I) Morphological effects of air-exposed development. (A, B, F, G)C. magdalenae. (C, H, I)C. brunneus. (D)L. frenatus. (E)C. kuelpmannii. Images are not to scale.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4016651&req=5

Figure 1: Upper row: developmental stages in Rivulus spp. (A) Stage one: approximately 50% epiboly; (B) Stage two: neural keel. (C) Stage three: optic cups; (D) Stage four: pigmentation in eyes and skin; (E) Stage five: embryo surrounding yolk sac. Lower row: (F-I) Morphological effects of air-exposed development. (A, B, F, G)C. magdalenae. (C, H, I)C. brunneus. (D)L. frenatus. (E)C. kuelpmannii. Images are not to scale.
Mentions: We collected 209 eggs from C. brunneus, 112 from C. magdalenae, 23 from C. kuelpmanni, 11 from A. immaculatus, and 10 eggs from L. frenatus (all 10 in the test group). Numbers of embryos that reached each developmental stage and numbers hatched are given per pair and per treatment in Table 1. The overall median time duration of the desiccation treatment among the embryos that were returned to water was 8 days (eight for C. brunneus, six for C. magdalenae). Effects of developing in air were visible few hours after the start of the treatment. Generally, after 48 hours egg envelopes became opaque and rough, depressions in the egg surface appeared and eggs started shrinking (Figure 1). However, these effects were variable in different embryos (see Figure 1I and H for embryos from the same clutch experiencing identical conditions). Few embryos were returned from the desiccation treatment into water before they reached stage three. Therefore, assuming a potential lack of power, we did not expect any significant period effects and effects of the duration of the dry period experienced for stages one and two. In none of the analysis, rates in the Test and Control groups were different and we pooled these groups for the presentation of results. We therefore only present Control and Desiccation treatment levels.

Bottom Line: We have estimated effects on developmental and mortality rates during and after the desiccation treatment.Embryos of these non-annual rivulids decreased their developmental rates in early stages of development in response to desiccation and this effect persisted after the treatment.In one of these, we found cohorts of embryos in the latest stages of development that did not hatch over a period of more than 1 month without mortality.

View Article: PubMed Central - HTML - PubMed

Affiliation: Naturalis Biodiversity Center, Darwinweg 2, Leiden 2333 CR, The Netherlands ; Current address: Instituto Gulbenkian de Ciência, Rua da Quinta Grande 6, 2780-156 Oeiras, Portugal.

ABSTRACT

Background: Diapause is a developmental arrest present in annual killifish, whose eggs are able to survive long periods of desiccation when the temporary ponds they inhabit dry up. Diapause can occur in three different developmental stages. These differ, within and between species, in their responsiveness to different environmental cues. A role of developmental plasticity and genetic assimilation in diapause evolution has been previously suggested but not experimentally explored. We investigated whether plastic developmental delays or arrests provoked by an unusual and extreme environment could be the ancestral condition for diapause. This would be in agreement with plasticity evolution playing a role in the emergence of diapause in this group. We have used a comparative experimental approach and exposed embryos of non-annual killifish belonging to five different species from the former genus Rivulus to brief periods of desiccation. We have estimated effects on developmental and mortality rates during and after the desiccation treatment.

Results: Embryos of these non-annual rivulids decreased their developmental rates in early stages of development in response to desiccation and this effect persisted after the treatment. Two pairs of two different species had sufficient sample sizes to investigate rates of development in later stages well. In one of these, we found cohorts of embryos in the latest stages of development that did not hatch over a period of more than 1 month without mortality. Several properties of this arrest are also used to characterize diapause III in annual killifish. Such a cohort is present in control conditions and increases in frequency in the desiccation treatment.

Conclusions: The presence of plasticity for developmental timing and a prolonged developmental arrest in non-annual rivulids, suggest that a plastic developmental delay or diapause might have been present in the shared ancestor of annual and non-annual South American killifish and that the evolution of plasticity could have played a role in the emergence of the diapauses. Further comparative experimental studies and field research are needed to better understand how diapause and its plasticity evolved in this group.

No MeSH data available.


Related in: MedlinePlus