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Effects of population outcrossing on rotifer fitness.

Tortajada AM, Carmona MJ, Serra M - BMC Evol. Biol. (2010)

Bottom Line: Outcrossing between populations can exert either positive or negative effects on offspring fitness.Fitness of the outcrossed offspring was compared with fitness of the offspring of the reference population for both generations and for three different between-population combinations.In newly-founded populations, where the population size is still small, dilution of immigrants should be low.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institut Cavanilles de Biodiversitat i Biologia Evolutiva, Universitat de València, A,O, 22085, València 46071, Spain. ana.maria.tortajada@uv.es

ABSTRACT

Background: Outcrossing between populations can exert either positive or negative effects on offspring fitness. Cyclically parthenogenetic rotifers, like other continental zooplankters, show high genetic differentiation despite their high potential for passive dispersal. Within this context, the effects of outcrossing may be relevant in modulating gene flow between populations through selection for or against interpopulation hybrids. Nevertheless, these effects remain practically unexplored in rotifers. Here, the consequences of outcrossing on the rotifer Brachionus plicatilis were investigated. Cross-mating experiments were performed between a reference population and three alternative populations that differed in their genetic distance with regard to the former. Two offspring generations were obtained: F1 and BC ('backcross'). Fitness of the outcrossed offspring was compared with fitness of the offspring of the reference population for both generations and for three different between-population combinations. Four fitness components were measured throughout the rotifer life cycle: the diapausing egg-hatching proportion, clone viability (for the clones originating from diapausing eggs), initial net growth rate R for each viable clone, and the proportion of male-producing clones. Additionally, both the parental fertilisation proportion and a compound fitness measure, integrating the complete life cycle, were estimated.

Results: In the F1 generation, hybrid vigour was detected for the diapausing egg-hatching proportion, while R was lower in the outcrossed offspring than in the offspring of the reference population. Despite these contrasting results, hybrid vigour was globally observed for the compound measure of fitness. Moreover, there was evidence that this vigour could increase with the genetic differentiation of the outcrossed populations. In the BC generation, the hybrid vigour detected for the egg-hatching proportion in the F1 generation reverted to outbreeding depression. By contrast, signs of hybrid vigour were observed for clone viability and R. The opposing trends observed for different life-cycle stages yielded a global pattern of hybrid vigour in the BC generation for two out of the three between-population comparisons.

Conclusions: Results suggest that outbreeding depression does not constitute a barrier to gene flow. In newly-founded populations, where the population size is still small, dilution of immigrants should be low. Thus, a lack of outbreeding depression would allow gene flow to have an impact on the genetic composition of these populations.

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Design of cross-mating experiments to obtain F1 and BC generations, performed with four B. plicatilis populations. TOS population was regarded as a resident population and the other three (HOS, TUR and CHI) as alternative immigrant source populations. N is the number of eggs tested for hatching.
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Figure 1: Design of cross-mating experiments to obtain F1 and BC generations, performed with four B. plicatilis populations. TOS population was regarded as a resident population and the other three (HOS, TUR and CHI) as alternative immigrant source populations. N is the number of eggs tested for hatching.

Mentions: The cyclically parthenogenetic rotifer Brachionus plicatilis (Müller 1786) is a model species in ecological genetics and population ecology [e.g. [10,26]]. In this study, individuals of B. plicatilis from different populations were crossed to investigate the effect on offspring fitness. The objective was to shed light on the consequences of between-population outbreeding on gene flow. The experimental design tried to mimic the sequence of crosses that would be likely to occur in a large (not newly-founded) population after the arrival of immigrant individuals, so it focused on the crosses that would offer the opportunity for immigrant genes to be introduced into the resident population. Four B. plicatilis populations (acronyms: TOS, HOS, TUR and CHI; see Methods for details) were selected. TOS was regarded as a resident population where immigrants would arrive, and the other three were alternative immigrant source populations. Crosses between clones from these populations were conducted in the laboratory, and offspring fitness from intra- and interpopulation crosses was estimated by measuring life-history traits throughout the rotifer life cycle, from the diapausing-egg stage to the induction of sexual reproduction. Furthermore, the number of females obtained per incubated diapausing egg at the end of the experiment was used as a compound fitness measure. Additionally, the parental fertilisation proportion was estimated from the cross-mating experiments. As the negative effects of outbreeding often do not appear until the second generation [5], backcrosses were carried out to obtain a backcross (BC) generation. For backcrosses, two types of crosses were compared: (1) crosses between the F1 'resident × immigrant hybrids' and 'resident' clones (hereafter, hybrid-resident); and (2) crosses between the F1 'resident × resident' and 'resident' clones (hereafter, resident-resident; Figure 1). A clone was not used in more than one cross. The 'immigrant × immigrant' crosses were not tested, as they were assumed to be unlikely to occur in nature due to the dilution of immigrants in a large population of residents. Zooplankton mobility (i.e., vertical migration) and water column turbulence make spatial clustering of relatives improbable, thus reducing the chances of mating among the parthenogenetic offspring of an immigrant.


Effects of population outcrossing on rotifer fitness.

Tortajada AM, Carmona MJ, Serra M - BMC Evol. Biol. (2010)

Design of cross-mating experiments to obtain F1 and BC generations, performed with four B. plicatilis populations. TOS population was regarded as a resident population and the other three (HOS, TUR and CHI) as alternative immigrant source populations. N is the number of eggs tested for hatching.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2967546&req=5

Figure 1: Design of cross-mating experiments to obtain F1 and BC generations, performed with four B. plicatilis populations. TOS population was regarded as a resident population and the other three (HOS, TUR and CHI) as alternative immigrant source populations. N is the number of eggs tested for hatching.
Mentions: The cyclically parthenogenetic rotifer Brachionus plicatilis (Müller 1786) is a model species in ecological genetics and population ecology [e.g. [10,26]]. In this study, individuals of B. plicatilis from different populations were crossed to investigate the effect on offspring fitness. The objective was to shed light on the consequences of between-population outbreeding on gene flow. The experimental design tried to mimic the sequence of crosses that would be likely to occur in a large (not newly-founded) population after the arrival of immigrant individuals, so it focused on the crosses that would offer the opportunity for immigrant genes to be introduced into the resident population. Four B. plicatilis populations (acronyms: TOS, HOS, TUR and CHI; see Methods for details) were selected. TOS was regarded as a resident population where immigrants would arrive, and the other three were alternative immigrant source populations. Crosses between clones from these populations were conducted in the laboratory, and offspring fitness from intra- and interpopulation crosses was estimated by measuring life-history traits throughout the rotifer life cycle, from the diapausing-egg stage to the induction of sexual reproduction. Furthermore, the number of females obtained per incubated diapausing egg at the end of the experiment was used as a compound fitness measure. Additionally, the parental fertilisation proportion was estimated from the cross-mating experiments. As the negative effects of outbreeding often do not appear until the second generation [5], backcrosses were carried out to obtain a backcross (BC) generation. For backcrosses, two types of crosses were compared: (1) crosses between the F1 'resident × immigrant hybrids' and 'resident' clones (hereafter, hybrid-resident); and (2) crosses between the F1 'resident × resident' and 'resident' clones (hereafter, resident-resident; Figure 1). A clone was not used in more than one cross. The 'immigrant × immigrant' crosses were not tested, as they were assumed to be unlikely to occur in nature due to the dilution of immigrants in a large population of residents. Zooplankton mobility (i.e., vertical migration) and water column turbulence make spatial clustering of relatives improbable, thus reducing the chances of mating among the parthenogenetic offspring of an immigrant.

Bottom Line: Outcrossing between populations can exert either positive or negative effects on offspring fitness.Fitness of the outcrossed offspring was compared with fitness of the offspring of the reference population for both generations and for three different between-population combinations.In newly-founded populations, where the population size is still small, dilution of immigrants should be low.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institut Cavanilles de Biodiversitat i Biologia Evolutiva, Universitat de València, A,O, 22085, València 46071, Spain. ana.maria.tortajada@uv.es

ABSTRACT

Background: Outcrossing between populations can exert either positive or negative effects on offspring fitness. Cyclically parthenogenetic rotifers, like other continental zooplankters, show high genetic differentiation despite their high potential for passive dispersal. Within this context, the effects of outcrossing may be relevant in modulating gene flow between populations through selection for or against interpopulation hybrids. Nevertheless, these effects remain practically unexplored in rotifers. Here, the consequences of outcrossing on the rotifer Brachionus plicatilis were investigated. Cross-mating experiments were performed between a reference population and three alternative populations that differed in their genetic distance with regard to the former. Two offspring generations were obtained: F1 and BC ('backcross'). Fitness of the outcrossed offspring was compared with fitness of the offspring of the reference population for both generations and for three different between-population combinations. Four fitness components were measured throughout the rotifer life cycle: the diapausing egg-hatching proportion, clone viability (for the clones originating from diapausing eggs), initial net growth rate R for each viable clone, and the proportion of male-producing clones. Additionally, both the parental fertilisation proportion and a compound fitness measure, integrating the complete life cycle, were estimated.

Results: In the F1 generation, hybrid vigour was detected for the diapausing egg-hatching proportion, while R was lower in the outcrossed offspring than in the offspring of the reference population. Despite these contrasting results, hybrid vigour was globally observed for the compound measure of fitness. Moreover, there was evidence that this vigour could increase with the genetic differentiation of the outcrossed populations. In the BC generation, the hybrid vigour detected for the egg-hatching proportion in the F1 generation reverted to outbreeding depression. By contrast, signs of hybrid vigour were observed for clone viability and R. The opposing trends observed for different life-cycle stages yielded a global pattern of hybrid vigour in the BC generation for two out of the three between-population comparisons.

Conclusions: Results suggest that outbreeding depression does not constitute a barrier to gene flow. In newly-founded populations, where the population size is still small, dilution of immigrants should be low. Thus, a lack of outbreeding depression would allow gene flow to have an impact on the genetic composition of these populations.

Show MeSH
Related in: MedlinePlus