Oecologia (2001) 128:379–388 DOI 10.1007/s004420100674
Charles-Antoine Dedryver · Maurice Hullé Jean-François Le Gallic · Marina C. Caillaud Jean-Christophe Simon
Coexistence in space and time of sexual and asexual populations of the cereal aphid Sitobion avenae Received: 18 October 2000 / Accepted: 12 February 2001 / Published online: 19 April 2001 © Springer-Verlag 2001
Abstract Aphids typically reproduce by cyclical parthenogenesis, with a single sexual generation alternating with numerous asexual generations each year. However, some species exhibit different life cycle variants with various degrees of investment in sexuality. We tested the hypothesis that these life cycle variants are selected in space and time by climatic factors, mainly winter severity, due to an ecological link between sexual reproduction and the production of a cold-resistant form, the egg. More than 600 clones of the aphid Sitobion avenae F. were collected in five to six regions of France with contrasting climates during 3 consecutive years and compared for their production of sexual forms in standardised conditions. As predicted by a recent model of breeding system distribution and maintenance in aphids, we found a clear shift between northern and southern populations, with decreasing sexuality southwards. Life cycle variants investing entirely or partly in sexual reproduction in autumn predominated in northern sites, while obligate parthenogens and male-producers dominated in the southern sites. No clear east–west pattern of decreasing sexuality was found, and annualvariation in the relative proportions of life cycle variants was not clearly influenced by the severity of the previous winter. These latter results suggest that other selection pressures could interact with winter climate to determine the local life cycle polymorphism in S. avenae populations. Keywords Aphididae · Cyclical parthenogenesis · Sex evolution · Clone · France
C.-A. Dedryver (✉) · M. Hullé · J.-F. Le Gallic · J.-C. Simon INRA/ENSA,Unité Mixte de Recherche Biologie des Organismes et des Populations appliquée à la Protection des Plantes (BiO3P), Domaine de la Motte, B.P. 35327, 35653 Le Rheu cedex, France e-mail: [email protected] Tel.: +33-223-485151, Fax: +33-223-485150 M. C. Caillaud Cornell University, Department of Entomology, Comstock Hall, Ithaca, NY 14853, USA
Introduction The coexistence of sexual and parthenogenetic forms within the same species is not rare in nature (Suomalainen 1950). Understanding how this breeding system variation is maintained remains a widely debated question in ecology and evolutionary biology (Stearns 1990; Kondrashov 1993; Michod 1995; Hurst and Peck 1996; Sunnucks et al. 1997, 1998; Rispe et al. 1998a). Studies in this field often address the differential distribution of both reproductive categories (as for example the “geographic parthenogenesis” concept of Vandel 1928). Geographic parthenogenesis is usually thought to reflect different responses to selection pressures associated with spatial patterning of abiotic and biotic environmental factors, especially climatic ones (Lynch 1984). In plant species, asexual lineages generally tend to replace sexual lineages in cold climates, i.e. at higher latitudes or altitudes (Peck et al. 1998). For some invertebrates like weevils (Suomalainen 1950) and Daphnia (Hebert et al. 1993), parthenogenetic lineages were observed to occur in more unfavourable conditions than did sexual ones. The dominance of parthenogens in harsh environments is generally thought to be due to strong pressures selecting optimally adapted genotypes which are not susceptible to breakage by recombination, as would occur during sexual reproduction (Peck et al. 1998). However, interpretation of such systems is often confounded by the ploidy level shifts that usually accompany breeding system transitions (Suomalainen 1950; Dufresne and Hebert 1994). Nevertheless, if disjunct distributions are known for many sexual-asexual complexes, the coexistence of asexual variants with their sexual relatives on a microgeographic scale (e.g. Daphnia pulex in the same pond, aphids in the same field) has been noted several times (Lynch 1984; Hebert et al. 1993; Simon et al. 1996; Dedryver et al. 1998b). Cyclical parthenogens typically show an alternation of sexual and parthenogenetic generations which, in theory, combines the advantages of both types of reproduction: sexuality generates new genotypes while partheno-
380
genesis allows rapid multiplication of the best-fitted ones. The sexual phase can also be facultative or lost by some genotypes, and populations of such organisms are often a mixture of obligate and cyclical parthenogenetic lines (Hebert et al. 1993). Among cyclical parthenogenetic organisms, aphids present several biological features making them useful models for assessing the extent of geographic parthenogenesis and the conditions of maintenance or exclusion of life cycle polymorphism in animal populations. First, during their apomictic parthenogenetic phase (most of the year), aphid populations consist of a mixture of different clones each producing numerous copies of the same genotype. Second, they produce wingless and winged parthenogenetic individuals, the latter conferring a high dispersal potential that may prevent local adaptation. Third, their ancestral mode of reproduction is cyclical parthenogenesis; in the annual life cycle, numerous parthenogenetic generations are followed by a single sexual generation in autumn which, in most species, is triggered by decreasing photoperiod and temperature (Bonnemaison 1951). Nevertheless, clones exhibiting different modes of reproduction from cyclicto obligate parthenogenesis may coexist within the same species, without a ploidy level shift. Holocyclic clones retain a full commitment to sexual reproduction once a year, with bouts of asexuality followed by the generation of only males and sexual females that lay fertilised diapausing eggs in the autumn. Intermediate clones continue to produce parthenogenetic individuals in autumn but also a full array of sexual forms (Blackman 1971). Androcyclic clones produce only parthenogenetic forms as well as males in autumn. Anholocyclics have abandoned sexual reproduction, reproducing all the year round by sustained parthenogenesis (Blackman 1971; MacKay 1989; Dedryver et al. 1998b). Fourth, most parthenogenetic individuals are eliminated by temperatures below –5 to –10°C, depending on species (Williams 1980) and only fertilised eggs can resist long periods of intense frost (Sømme 1969). This link between sexuality and cold resistance can be seen as a contingent short-term advantage for sex (Rispe et al. 1998a). Genotypes investing in a single reproductive strategy (sex or parthenogenesisonly) are likely to be favoured in areas where winters are regularly either cold (holocyclic clones) or mild (anholocyclic clones). Genotypes investing in both strategies (intermediates or androcyclics) may be favoured in areas where winter climate fluctuates around the threshold for the survival of parthenogenetic individuals (i.e. most western Europe countries) by limiting the risk of low fitness in an unpredictable climate (Dedryver et al. 1998b). A result of these selective patterns is that geographic parthenogenesis in aphids is “upside-down” compared to most organisms which have more parthenogenesis northwards (Hughes 1989). In the present study, we investigated the variation in abundance of the different breeding systems occurring
in an aphid species over 3 years and six regions of France with contrasting winter climates. Our aim was to test the hypothesis of their selection by climatic factors with reference to Rispe models (Rispe and Pierre 1998; Rispe et al. 1998a) predicting (1) decreasing sexuality along climatic gradients in Europe from the cold continental east to the mild oceanic west and similar gradients from north to south, and (2) maintenance of breeding system polymorphism in areas with fluctuating winter climate. We used the non-host-alternating aphid Sitobion avenae F. (Aphididae, Sternorrhyncha), which is an important pest of cereals worldwide due to its sap feeding and virus transmission (LeclercqLe Quillec et al. 1995; Plantegenest et al. 1996). S. avenae exhibits a high level of phenotypic diversity, including life cycle variation. It possesses a wide range of breeding systems (holocyclics, intermediates, androcyclics, anholocyclics), and gene flow occurs between holocyclics, intermediates and androcyclics, at least in laboratory experiments (Dedryver et al. 1998b; Simon et al. 1999). S. avenae also displays variation in host plant preferences (Caillaud et al. 1995; De Barro et al. 1995a, 1995b; Sunnucks et al. 1997; Haack et al. 2000) and colour polymorphism, with clones varying from pale green to dark brown (Lowe 1981; Weber 1985; Dedryver et al. 1994). A recent study using microsatellite markers showed strong genetic differentiation between northern and southern populations of S. avenae in France, likely resulting from geographic partitioning of breeding system variation (Simon et al. 1999). The present study confirms on a larger spatiotemporal scale the importance of climate in structuring life cycle polymorphism.
Materials and methods Aphid collections Parthenogenetic females of S. avenae were collected in April 1993, 1994 and 1995 from five regions of France with contrasting winter climates (Table 1, Fig. 1): Nord and Champagne, in the north and in the north-east of the country, respectively, with a high (≥50) annual mean number of frost days (minimal daily temperatures below 0°C) and low winter minimal temperatures (less than –10°C on average), Normandie and Bretagne, in the north-west, with 30 frost days on average and mean minimal winter temperatures of –7.6°C, and Languedoc in southern France, with a low mean number of frost days and a minimal winter temperature around –5°C, typical for a Mediterranean climate. An additional collection was made in Provence (south-east; with a climate similarto Languedoc) in April 1995. Aphid collections were also made in Nord, Champagne, Normandie and Bretagne in July 1994. In all sampled regions, graminaceous crops (cereals, maize and temporary grass pastures) are planted on a large portion of the arable land (85.5% in Bretagne, 81.4% in Normandie, 64.5% in Nord, 58.4% in Champagne, 46% in Languedoc and 42% in Provence). Wheat is the most cultivated cereal everywhere (from 17.4% of arable land in Bretagne to 40.2% in Nord), more barley is grown in Champagne and Nord (16% and 10% of arable land, respectively) than in other regions. Maize and temporary grass pastures are particularly abundant in Normandie (33% and 15%, respectively) and Bretagne (30% and 33%, respectively).
381 Table 1 Number of frost days, absolute minimal temperature in °C (in parentheses) and cumulated negative temperatures (in italics) registered from November to March of 1992–1993, 1993–1994 and 1994–1995, and the mean for 1982–1996 at five sites representative of the main sampled regions [N–8 frequency of winters with minimal absolute temperature
Charles-Antoine Dedryver · Maurice Hullé Jean-François Le Gallic · Marina C. Caillaud Jean-Christophe Simon
Coexistence in space and time of sexual and asexual populations of the cereal aphid Sitobion avenae Received: 18 October 2000 / Accepted: 12 February 2001 / Published online: 19 April 2001 © Springer-Verlag 2001
Abstract Aphids typically reproduce by cyclical parthenogenesis, with a single sexual generation alternating with numerous asexual generations each year. However, some species exhibit different life cycle variants with various degrees of investment in sexuality. We tested the hypothesis that these life cycle variants are selected in space and time by climatic factors, mainly winter severity, due to an ecological link between sexual reproduction and the production of a cold-resistant form, the egg. More than 600 clones of the aphid Sitobion avenae F. were collected in five to six regions of France with contrasting climates during 3 consecutive years and compared for their production of sexual forms in standardised conditions. As predicted by a recent model of breeding system distribution and maintenance in aphids, we found a clear shift between northern and southern populations, with decreasing sexuality southwards. Life cycle variants investing entirely or partly in sexual reproduction in autumn predominated in northern sites, while obligate parthenogens and male-producers dominated in the southern sites. No clear east–west pattern of decreasing sexuality was found, and annualvariation in the relative proportions of life cycle variants was not clearly influenced by the severity of the previous winter. These latter results suggest that other selection pressures could interact with winter climate to determine the local life cycle polymorphism in S. avenae populations. Keywords Aphididae · Cyclical parthenogenesis · Sex evolution · Clone · France
C.-A. Dedryver (✉) · M. Hullé · J.-F. Le Gallic · J.-C. Simon INRA/ENSA,Unité Mixte de Recherche Biologie des Organismes et des Populations appliquée à la Protection des Plantes (BiO3P), Domaine de la Motte, B.P. 35327, 35653 Le Rheu cedex, France e-mail: [email protected] Tel.: +33-223-485151, Fax: +33-223-485150 M. C. Caillaud Cornell University, Department of Entomology, Comstock Hall, Ithaca, NY 14853, USA
Introduction The coexistence of sexual and parthenogenetic forms within the same species is not rare in nature (Suomalainen 1950). Understanding how this breeding system variation is maintained remains a widely debated question in ecology and evolutionary biology (Stearns 1990; Kondrashov 1993; Michod 1995; Hurst and Peck 1996; Sunnucks et al. 1997, 1998; Rispe et al. 1998a). Studies in this field often address the differential distribution of both reproductive categories (as for example the “geographic parthenogenesis” concept of Vandel 1928). Geographic parthenogenesis is usually thought to reflect different responses to selection pressures associated with spatial patterning of abiotic and biotic environmental factors, especially climatic ones (Lynch 1984). In plant species, asexual lineages generally tend to replace sexual lineages in cold climates, i.e. at higher latitudes or altitudes (Peck et al. 1998). For some invertebrates like weevils (Suomalainen 1950) and Daphnia (Hebert et al. 1993), parthenogenetic lineages were observed to occur in more unfavourable conditions than did sexual ones. The dominance of parthenogens in harsh environments is generally thought to be due to strong pressures selecting optimally adapted genotypes which are not susceptible to breakage by recombination, as would occur during sexual reproduction (Peck et al. 1998). However, interpretation of such systems is often confounded by the ploidy level shifts that usually accompany breeding system transitions (Suomalainen 1950; Dufresne and Hebert 1994). Nevertheless, if disjunct distributions are known for many sexual-asexual complexes, the coexistence of asexual variants with their sexual relatives on a microgeographic scale (e.g. Daphnia pulex in the same pond, aphids in the same field) has been noted several times (Lynch 1984; Hebert et al. 1993; Simon et al. 1996; Dedryver et al. 1998b). Cyclical parthenogens typically show an alternation of sexual and parthenogenetic generations which, in theory, combines the advantages of both types of reproduction: sexuality generates new genotypes while partheno-
380
genesis allows rapid multiplication of the best-fitted ones. The sexual phase can also be facultative or lost by some genotypes, and populations of such organisms are often a mixture of obligate and cyclical parthenogenetic lines (Hebert et al. 1993). Among cyclical parthenogenetic organisms, aphids present several biological features making them useful models for assessing the extent of geographic parthenogenesis and the conditions of maintenance or exclusion of life cycle polymorphism in animal populations. First, during their apomictic parthenogenetic phase (most of the year), aphid populations consist of a mixture of different clones each producing numerous copies of the same genotype. Second, they produce wingless and winged parthenogenetic individuals, the latter conferring a high dispersal potential that may prevent local adaptation. Third, their ancestral mode of reproduction is cyclical parthenogenesis; in the annual life cycle, numerous parthenogenetic generations are followed by a single sexual generation in autumn which, in most species, is triggered by decreasing photoperiod and temperature (Bonnemaison 1951). Nevertheless, clones exhibiting different modes of reproduction from cyclicto obligate parthenogenesis may coexist within the same species, without a ploidy level shift. Holocyclic clones retain a full commitment to sexual reproduction once a year, with bouts of asexuality followed by the generation of only males and sexual females that lay fertilised diapausing eggs in the autumn. Intermediate clones continue to produce parthenogenetic individuals in autumn but also a full array of sexual forms (Blackman 1971). Androcyclic clones produce only parthenogenetic forms as well as males in autumn. Anholocyclics have abandoned sexual reproduction, reproducing all the year round by sustained parthenogenesis (Blackman 1971; MacKay 1989; Dedryver et al. 1998b). Fourth, most parthenogenetic individuals are eliminated by temperatures below –5 to –10°C, depending on species (Williams 1980) and only fertilised eggs can resist long periods of intense frost (Sømme 1969). This link between sexuality and cold resistance can be seen as a contingent short-term advantage for sex (Rispe et al. 1998a). Genotypes investing in a single reproductive strategy (sex or parthenogenesisonly) are likely to be favoured in areas where winters are regularly either cold (holocyclic clones) or mild (anholocyclic clones). Genotypes investing in both strategies (intermediates or androcyclics) may be favoured in areas where winter climate fluctuates around the threshold for the survival of parthenogenetic individuals (i.e. most western Europe countries) by limiting the risk of low fitness in an unpredictable climate (Dedryver et al. 1998b). A result of these selective patterns is that geographic parthenogenesis in aphids is “upside-down” compared to most organisms which have more parthenogenesis northwards (Hughes 1989). In the present study, we investigated the variation in abundance of the different breeding systems occurring
in an aphid species over 3 years and six regions of France with contrasting winter climates. Our aim was to test the hypothesis of their selection by climatic factors with reference to Rispe models (Rispe and Pierre 1998; Rispe et al. 1998a) predicting (1) decreasing sexuality along climatic gradients in Europe from the cold continental east to the mild oceanic west and similar gradients from north to south, and (2) maintenance of breeding system polymorphism in areas with fluctuating winter climate. We used the non-host-alternating aphid Sitobion avenae F. (Aphididae, Sternorrhyncha), which is an important pest of cereals worldwide due to its sap feeding and virus transmission (LeclercqLe Quillec et al. 1995; Plantegenest et al. 1996). S. avenae exhibits a high level of phenotypic diversity, including life cycle variation. It possesses a wide range of breeding systems (holocyclics, intermediates, androcyclics, anholocyclics), and gene flow occurs between holocyclics, intermediates and androcyclics, at least in laboratory experiments (Dedryver et al. 1998b; Simon et al. 1999). S. avenae also displays variation in host plant preferences (Caillaud et al. 1995; De Barro et al. 1995a, 1995b; Sunnucks et al. 1997; Haack et al. 2000) and colour polymorphism, with clones varying from pale green to dark brown (Lowe 1981; Weber 1985; Dedryver et al. 1994). A recent study using microsatellite markers showed strong genetic differentiation between northern and southern populations of S. avenae in France, likely resulting from geographic partitioning of breeding system variation (Simon et al. 1999). The present study confirms on a larger spatiotemporal scale the importance of climate in structuring life cycle polymorphism.
Materials and methods Aphid collections Parthenogenetic females of S. avenae were collected in April 1993, 1994 and 1995 from five regions of France with contrasting winter climates (Table 1, Fig. 1): Nord and Champagne, in the north and in the north-east of the country, respectively, with a high (≥50) annual mean number of frost days (minimal daily temperatures below 0°C) and low winter minimal temperatures (less than –10°C on average), Normandie and Bretagne, in the north-west, with 30 frost days on average and mean minimal winter temperatures of –7.6°C, and Languedoc in southern France, with a low mean number of frost days and a minimal winter temperature around –5°C, typical for a Mediterranean climate. An additional collection was made in Provence (south-east; with a climate similarto Languedoc) in April 1995. Aphid collections were also made in Nord, Champagne, Normandie and Bretagne in July 1994. In all sampled regions, graminaceous crops (cereals, maize and temporary grass pastures) are planted on a large portion of the arable land (85.5% in Bretagne, 81.4% in Normandie, 64.5% in Nord, 58.4% in Champagne, 46% in Languedoc and 42% in Provence). Wheat is the most cultivated cereal everywhere (from 17.4% of arable land in Bretagne to 40.2% in Nord), more barley is grown in Champagne and Nord (16% and 10% of arable land, respectively) than in other regions. Maize and temporary grass pastures are particularly abundant in Normandie (33% and 15%, respectively) and Bretagne (30% and 33%, respectively).
381 Table 1 Number of frost days, absolute minimal temperature in °C (in parentheses) and cumulated negative temperatures (in italics) registered from November to March of 1992–1993, 1993–1994 and 1994–1995, and the mean for 1982–1996 at five sites representative of the main sampled regions [N–8 frequency of winters with minimal absolute temperature
