Widespread Host-Dependent Hybrid Unfitness in the Pea Aphid Species Complex

Peccoud, Jean; Huerta, Manon de la; Bonhomme, Joël; Laurence, Cindy; Outreman, Yannick; Smadja, Carole

doi:10.1111/evo.12478

Cited by 28 publications

(36 citation statements)

References 77 publications

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“…For pea aphid, V. faba represents such a universal host. In our study, we found little evidence for reduced hybrid fitness on V. faba compared with parental genotypes, consistent with the findings of Peccoud et al (2014) across a wide range of F 1 populations derived from crosses between and within species-level biotypes. Nonetheless, we cannot exclude the possibility that at the initial stage of F 1 clonal colony establishment, some fundatrices may have failed to thrive.…”

Section: Evolution Of Virulencesupporting

confidence: 88%

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Cryptic Virulence and Avirulence Alleles Revealed by Controlled Sexual Recombination in Pea Aphids

et al. 2014

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Although aphids are worldwide crop pests, little is known about aphid effector genes underlying virulence and avirulence. Here we show that controlling the genetics of both aphid and host can reveal novel recombinant genotypes with previously undetected allelic variation in both virulence and avirulence functions. Clonal F 1 progeny populations were derived from reciprocal crosses and self-matings between two parental genotypes of pea aphid (Acyrthosiphon pisum) differing in virulence on a Medicago truncatula host carrying the RAP1 and RAP2 resistance genes. These populations showed Mendelian segregation consistent with aphid performance being controlled largely by a dominant virulence allele derived from only one parent. Altered segregation ratios on near-isogenic host genotypes differing in the region carrying RAP1 were indicative of additional heritable functions likely related to avirulence genes originating from both parents. Unexpectedly, some virulent F 1 progeny were recovered from selfing of an avirulent parent, suggesting a reservoir of cryptic alleles. Host chlorosis was associated with virulence, whereas necrotic hypersensitive-like response was not. No maternal inheritance was found for any of these characteristics, ruling out sex-linked, cytoplasmic, and endosymbiotic factors. Our results demonstrate the tractability of dissecting the genetic basis of pest-host resistance mechanisms and indicate that the annual sexual cycle in aphids may lead to frequent novel genotypes with both increased and decreased virulence. Availability of genomes for both pest and host can facilitate definition of cognate gene-for-gene relationships, potentially leading to selection of crop genotypes with multiple resistance traits. KEYWORDS aphid; virulence; avirulence; F 1 hybrid; near-isogenic line; R gene; gene-for-gene interaction; effector A BOUT 250 of the 4400 known species of aphids feed on agricultural crops (Oerke et al. 1994;Blackman and Eastop 2000). Given their wide host ranges and high fecundity, aphids can have dramatic negative impacts on host plants (Dixon 1987). Aphids feed specifically from phloem sieve elements, causing damage directly by ingestion of plant nutrients and by acting as vectors of many major plant viruses (Ng and Perry 2004). In many instances, aphids may manipulate or evade host defenses by secretion of saliva into phloem sieve elements and by minimizing cellular damage by moving their stylets along intercellular paths (Miles 1999;Will et al. 2007).Aphids have unusual reproductive cycles, typically with numerous asexual parthenogenetic generations followed by one sexual phase in winter (Via 1992). Novel genetic diversity may be subsequently stably propagated through asexual parthenogenetic lineages (Blackman 1985). Aphid populations harbor a considerable amount of genetic variability (Via 1989(Via , 1991aBlack et al. 1992), and cyclic parthenogens can evolve nearly as fast as species with sexual reproduction each generation (Lynch and Gabriel 1983). The genetic variation arising ...

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Section: Evolution Of Virulencesupporting

confidence: 88%

“…Low virulence of hybrid aphids potentially also could be due to intrinsic unfitness, defined by Peccoud et al (2014) as poor performance on a known highly compatible host. For pea aphid, V. faba represents such a universal host.…”

Section: Evolution Of Virulencementioning

confidence: 99%

Cryptic Virulence and Avirulence Alleles Revealed by Controlled Sexual Recombination in Pea Aphids

et al. 2014

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“…), or postzygotic, where hybrid performance depends on environmental conditions (e.g., Peccoud et al. ; Favre et al. ).…”

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confidence: 99%

Ecological divergence plays an important role in strong but complex reproductive isolation in campions (Silene)*

et al. 2018

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New species arise through the evolution of reproductive barriers between formerly interbreeding lineages. Yet, comprehensive assessments of potential reproductive barriers, which are needed to make inferences on processes driving speciation, are only available for a limited number of systems. In this study, we estimated individual and cumulative strengths of seven prezygotic and six postzygotic reproductive barriers between the recently diverged taxa Silene dioica (L.) Clairv. and S. latifolia Poiret using both published and new data. A combination of multiple partial reproductive barriers resulted in near‐complete reproductive isolation between S. dioica and S. latifolia, consistent with earlier estimates of gene flow between the taxa. Extrinsic barriers associated with adaptive ecological divergence were most important, while intrinsic postzygotic barriers had moderate individual strength but contributed only little to total reproductive isolation. These findings are in line with ecological divergence as driver of speciation. We further found extensive variation in extrinsic reproductive isolation, ranging from sites with very strong selection against migrants and hybrids to intermediate sites where substantial hybridization is possible. This situation may allow for, or even promote, heterogeneous genetic divergence.

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“…Loci involved in nonecological reproductive isolation between races, which may have evolved after specialization to different hosts, could also have been pinpointed by our genome scan (Bierne et al., ; Cruickshank & Hahn, ). As yet, no such form of reproductive isolation has been identified in pea aphids (Peccoud & Simon, ; Peccoud et al., ).…”

Section: Discussionmentioning

confidence: 99%

Identifying genomic hotspots of differentiation and candidate genes involved in the adaptive divergence of pea aphid host races

et al. 2018

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Identifying the genomic bases of adaptation to novel environments is a long-term objective in evolutionary biology. Because genetic differentiation is expected to increase between locally adapted populations at the genes targeted by selection, scanning the genome for elevated levels of differentiation is a first step towards deciphering the genomic architecture underlying adaptive divergence. The pea aphid Acyrthosiphon pisum is a model of choice to address this question, as it forms a large complex of plant-specialized races and cryptic species, resulting from recent adaptive radiation. Here, we characterized genomewide polymorphisms in three pea aphid races specialized on alfalfa, clover and pea crops, respectively, which we sequenced in pools (poolseq). Using a model-based approach that explicitly accounts for selection, we identified 392 genomic hotspots of differentiation spanning 47.3 Mb and 2,484 genes (respectively, 9.12% of the genome size and 8.10% of its genes). Most of these highly differentiated regions were located on the autosomes, and overall differentiation was weaker on the X chromosome. Within these hotspots, high levels of absolute divergence between races suggest that these regions experienced less gene flow than the rest of the genome, most likely by contributing to reproductive isolation. Moreover, population-specific analyses showed evidence of selection in every host race, depending on the hotspot considered. These hotspots were significantly enriched for candidate gene categories that control host-plant selection and use. These genes encode 48 salivary proteins, 14 gustatory receptors, 10 odorant receptors, five P450 cytochromes and one chemosensory protein, which represent promising candidates for the genetic basis of host-plant specialization and ecological isolation in the pea aphid complex. Altogether, our findings open new research directions towards functional studies, for validating the role of these genes on adaptive phenotypes.

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Widespread Host-Dependent Hybrid Unfitness in the Pea Aphid Species Complex

Cited by 28 publications

References 77 publications

Cryptic Virulence and Avirulence Alleles Revealed by Controlled Sexual Recombination in Pea Aphids

Cryptic Virulence and Avirulence Alleles Revealed by Controlled Sexual Recombination in Pea Aphids

Ecological divergence plays an important role in strong but complex reproductive isolation in campions (Silene)*

Identifying genomic hotspots of differentiation and candidate genes involved in the adaptive divergence of pea aphid host races

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