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

Abstract

The 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.

Diversification linked to larval host plant in the butterflyEumedonia eumedon

“…eumedon flies earlier in populations associated with the former (Figure 5). Similar to gall-forming wasps over distinct oak species (Zhang et al, 2019) and to the butterfly Phengaris arion (Bereczki et al, 2020;Bereczki et al, 2022), differences in breeding time between conspecific individuals (also known as allochrony) could act as a reproductive barrier between the populations found on G. sanguineum and G. subargenteum. The habitat preferences of the host plants probably strengthened isolation through habitat selection.…”

“…The multiple butterfly traits with significance for reproduction that can be modified by the use of alternative host plants (e.g., pheromones, colour, flight time, habitat choice) highlight the impact of host plants on the diversification of Lepidoptera as one of great significance, potentially at the level of factors such as adaptation to climate (e.g., Pitteloud et al, 2017 ) or reproductive interference (e.g., Hinojosa et al, 2020 ). Thus, the periodic publication of evidence of HAD in butterflies (Bereczki et al, 2020 ; Mikheyev et al, 2013 ; Nice & Shapiro, 2001 ) and moths (Joyce et al, 2016 ; Malausa et al, 2007 ; Silva‐Brandao et al, 2018 ) is not surprising. However, the available knowledge of HAD in Lepidoptera is still highly incomplete since it is unknown how common this phenomenon is across the lepidopteran tree of life, and cases are usually supported by weak genetic data, based on just one or a small set of markers.…”

“…This specialization can trigger adaptations causing isolation between populations. For example, differences in host plant phenologies can result in a barrier to gene flow by adult flight time modification and allochrony (Austin et al, 2008;Bereczki et al, 2020Bereczki et al, , 2022. Population differentiation can also be driven by the distinct chemistry of the host plants.…”

Population Genetic Structure and Demography of the Critically Endangered Chequered Blue Butterfly (Scolitantides orion) in a Highly Isolated Part of Its Distribution Range

“…Comparisons with studies on different species and using different microsatellite loci can be problematic. Nevertheless, it is worth noting that indices of genetic diversity were low but not extremely low when compared with other lycaenids, especially the most extensively studied Phengaris butterflies [ 60 , 61 , 62 , 63 , 64 ]. Therefore, although our ecological studies indicate some fluctuations in population sizes, genetic data did not indicate drastically reduced genetic variation in the studied populations.…”

Population genetic structure of a recent insect invasion: a gall midge, Asynapta groverae (Diptera: Cecidomyiidae) in South Korea since the first outbreak in 2008

“…Microsatellites, which are single sequence repeats, have been commonly used in population genetic studies on various insect taxa to identify genotypic diversity 35 , population genetic differentiation 36 , biological invasion [37][38][39] , host range expansion 40 , sexual selection 41 , ecological characteristics 42 , and speciation 43 . However, most microsatellites serve as species-specific markers.…”