Incipient sympatric speciation via host race formation in Phengaris arion (Lepidoptera: Lycaenidae)

AbstractThe plausibility of sympatric speciation is still debated despite increasing evidence, such as host races in insects. This speciation process may be occurring in the case of the two phenological forms of the obligatorily myrmecophilous Phengaris arion. The main goal of our research was to study the nature and causes of difference between these forms focusing primarily on the incipient speciation via host races. Molecular analyses based on highly variable microsatellites together with Wolbachia screening, male genitalia morphometrics and host ant studies were carried out on four syntopic sample pairs. Our results show that the two phenological forms of P. arion may meet the criteria for host plant races. They coexist in sympatry in certain parts of the species range which is allowed by the adaptation to the distinct phenology of the host plants. Negative selection acts against the intermediate individuals which are on the wing in the inappropriate time frame. Thus, disruptive selection affects and produces bimodal distributions of phenotypes. However, the phenology of food plants is not entirely distinct and fluctuates year by year. Therefore, the two forms can exchange genes occasionally depending on the length of the time slot when they can meet with each other. Consequently, the reproductive isolation could not be completed and the existence of the two arion forms may represent only an incipient stage of sympatric speciation. It is also clear that Wolbachia is likely not a driver of sympatric speciation in this case.

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Importance of the Life Cycle in Sympatric Host Race Formation and Speciation of Pathogens

Phytopathology ◽

10.1094/phyto-96-0280 ◽

2006 ◽

Vol 96 (3) ◽

pp. 280-287 ◽

Cited By ~ 70

Author(s):

Tatiana Giraud ◽

Lorys M. M. A. Villaréal ◽

Frédéric Austerlitz ◽

Mickaël Le Gac ◽

Claire Lavigne

Keyword(s):

Life Cycle ◽

Assortative Mating ◽

Plant Pathogens ◽

Species Concept ◽

Life Cycles ◽

Biological Species Concept ◽

Host Race ◽

Host Races ◽

Host Race Formation ◽

Race Formation

Numerous morphological species of pathogenic fungi have been shown to actually encompass several genetically isolated lineages, often specialized on different hosts and, thus, constituting host races or sibling species. In this article, we explore theoretically the importance of some aspects of the life cycle on the conditions of sympatric divergence of host races, particularly in fungal plant pathogens. Because the life cycles classically modeled by theoreticians of sympatric speciation correspond to those of free-living animals, sympatric divergence of host races requires the evolution of active assortative mating or of active host preference if mating takes place on the hosts. With some particular life cycles with restricted dispersal between selection on the host and mating, we show that divergence can occur in sympatry and lead to host race formation, or even speciation, by a mere process of specialization, with strong divergent adaptive selection. Neither active assortative mating nor active habitat choice is required in these cases, and this may explain why the phylo-genetic species concept seems more appropriate than the biological species concept in these organisms.

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Gall Flies, Inquilines, and Goldenrods: A Model for Host-race Formation and Sympatric Speciation

American Zoologist ◽

10.1093/icb/41.4.928 ◽

2001 ◽

Vol 41 (4) ◽

pp. 928-938 ◽

Cited By ~ 3

Author(s):

Warren G. Abrahamson ◽

Micky D. Eubanks ◽

Catherine P. Blair ◽

Amy V. Whipple

Keyword(s):

Sympatric Speciation ◽

Host Race ◽

Host Race Formation ◽

Race Formation

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Adaptive divergence and post-zygotic barriers to gene flow between sympatric populations of a herbivorous mite

Communications Biology ◽

10.1038/s42003-021-02380-y ◽

2021 ◽

Vol 4 (1) ◽

Author(s):

Ernesto Villacis-Perez ◽

Simon Snoeck ◽

Andre H. Kurlovs ◽

Richard M. Clark ◽

Johannes A. J. Breeuwer ◽

...

Keyword(s):

Gene Flow ◽

Plant Species ◽

Natural Setting ◽

Host Race ◽

Ecological Specialization ◽

Host Races ◽

Host Race Formation ◽

Herbivore Interactions ◽

Plant Herbivore ◽

Race Formation

AbstractPlant-herbivore interactions promote the generation and maintenance of both plant and herbivore biodiversity. The antagonistic interactions between plants and herbivores lead to host race formation: the evolution of herbivore types specializing on different plant species, with restricted gene flow between them. Understanding how ecological specialization promotes host race formation usually depends on artificial approaches, using laboratory experiments on populations associated with agricultural crops. However, evidence on how host races are formed and maintained in a natural setting remains scarce. Here, we take a multidisciplinary approach to understand whether populations of the generalist spider mite Tetranychus urticae form host races in nature. We demonstrate that a host race co-occurs among generalist conspecifics in the dune ecosystem of The Netherlands. Extensive field sampling and genotyping of individuals over three consecutive years showed a clear pattern of host associations. Genome-wide differences between the host race and generalist conspecifics were found using a dense set of SNPs on field-derived iso-female lines and previously sequenced genomes of T. urticae. Hybridization between lines of the host race and sympatric generalist lines is restricted by post-zygotic breakdown, and selection negatively impacts the survival of generalists on the native host of the host race. Our description of a host race among conspecifics with a larger diet breadth shows how ecological and reproductive isolation aid in maintaining intra-specific variation in sympatry, despite the opportunity for homogenization through gene flow. Our findings highlight the importance of explicitly considering the spatial and temporal scale on which plant-herbivore interactions occur in order to identify herbivore populations associated with different plant species in nature. This system can be used to study the underlying genetic architecture and mechanisms that facilitate the use of a large range of host plant taxa by extreme generalist herbivores. In addition, it offers the chance to investigate the prevalence and mechanisms of ecological specialization in nature.

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Evidence for Inversion Polymorphism Related to Sympatric Host Race Formation in the Apple Maggot Fly, Rhagoletis pomonella

Genetics ◽

10.1093/genetics/163.3.939 ◽

2003 ◽

Vol 163 (3) ◽

pp. 939-953 ◽

Cited By ~ 2

Author(s):

Jeffrey L Feder ◽

Joseph B Roethele ◽

Kenneth Filchak ◽

Julie Niedbalski ◽

Jeanne Romero-Severson

Keyword(s):

Sympatric Speciation ◽

Inversion Polymorphism ◽

Rhagoletis Pomonella ◽

Single Pair ◽

Host Race ◽

New Host ◽

Host Race Formation ◽

Allozyme Loci ◽

Genomic Regions ◽

Race Formation

Abstract Evidence suggests that the apple maggot, Rhagoletis pomonella (Diptera: Tephritidae) is undergoing sympatric speciation (i.e., divergence without geographic isolation) in the process of shifting and adapting to a new host plant. Prior to the introduction of cultivated apples (Malus pumila) in North America, R. pomonella infested the fruit of native hawthorns (Crataegus spp.). However, sometime in the mid-1800s the fly formed a sympatric race on apple. The recently derived apple-infesting race shows consistent allele frequency differences from the hawthorn host race for six allozyme loci mapping to three different chromosomes. Alleles at all six of these allozymes correlate with the timing of adult eclosion, an event dependent on the duration of the overwintering pupal diapause. This timing difference differentially adapts the univoltine fly races to an ∼3- to 4-week difference in the peak fruiting times of apple and hawthorn trees, partially reproductively isolating the host races. Here, we report finding substantial gametic disequilibrium among allozyme and complementary DNA (cDNA) markers encompassing the three chromosomal regions differentiating apple and hawthorn flies. The regions of disequilibrium extend well beyond the previously characterized six allozyme loci, covering substantial portions of chromosomes 1, 2, and 3 (haploid n = 6 in R. pomonella). Moreover, significant recombination heterogeneity and variation in gene order were observed among single-pair crosses for each of the three genomic regions, implying the existence of inversion polymorphism. We therefore have evidence that genes affecting diapause traits involved in host race formation reside within large complexes of rearranged genes. We explore whether these genomic regions (inversions) constitute coadapted gene complexes and discuss the implications of our findings for sympatric speciation in Rhagoletis.

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