Irma Wynhoff

Coevolutionary interactions between parasites and hosts are key drivers of biological adaptation. In this study, we explore the evolutionary response of the social parasitic butterfly Phengaris teleius to its host ant, Myrmica scabrinodis , taking advantage of a unique opportunity: the reintroduction of the butterfly in the Netherlands thirty years ago. We compared the degree of host mimicry and behavioural performance of caterpillars between the reintroduced and the Polish source population. After about thirty generations, chemical and vibroacoustical signal profiles have diverged. Chemical mimicry remained limited during the pre-adoption phase for both groups; however, in the post-adoption phase, the source population showed significantly higher chemical similarity to their local hosts. In contrast, reintroduced pre-adoption caterpillars evolved vibroacoustic signals closely resembling local hosts, also resulting in a stronger response from their local host ants. This suggests that adoption is driven by acoustics and subsequently serves as a selective filter promoting post-entry chemical refinement. Behavioural data evince that despite the differences between the different communication channels, the combination of signals remains sufficient to ensure recognition and integration in both host-parasite systems. These results illustrate how social parasites involved in multisensory mimicry can rapidly recalibrate strategies to remain functional in new ecological contexts.

Insect habitat specialists have declined more than generalists over the last decades. Understanding how habitat requirements and increased climate variability interact to explain persistence of populations is needed to enable effective conservation measures. Habitat specialists with a complex life cycle, such as myrmecophilous butterflies, are likely to be most vulnerable. Here, we explored to what extent the habitat factors explaining population persistence of the Alcon blue (Phengaris alcon), changed over a 25-year period in the Netherlands, contrasting the recent years 2018–2022 with extreme droughts with the preceding period 1998–2017 characterized by occasional climatic extremes. Population persistence of P. alcon over 1998–2017 as explained by historical habitat conditions was significantly higher in large heathland areas with large patches of its host plant Gentiana pneumonanthe. On the basis of current conditions, population persistence until 2017 was best explained by a combination of host plant area and quality. In contrast, persistence over the recent drought years was most closely associated with increasing occupancy of the optimal host ant Myrmica ruginodis and lower occupancy of competitive and predatory Lasius ants.Implications for insect conservation We conclude that critical habitat conditions change under increasing climatic extremes and that the availability of sufficient optimal host ants has become more critical than that of host plants. The results emphasise that both large-scale hydrological restoration and small-scale management for heterogeneity are necessary to preserve P. alcon and its habitat in the Netherlands. This is also likely to apply to other habitat specialists with complex life cycles from threatened habitats.

We review changes in the status of butterflies in Europe, focusing on long-running population data available for the United Kingdom, the Netherlands, and Belgium, based on standardized monitoring transects. In the United Kingdom, 8% of resident species have become extinct, and since 1976 overall numbers declined by around 50%. In the Netherlands, 20% of species have become extinct, and since 1990 overall numbers in the country declined by 50%. Distribution trends showed that butterfly distributions began decreasing long ago, and between 1890 and 1940, distributions declined by 80%. In Flanders (Belgium), 20 butterflies have become extinct (29%), and between 1992 and 2007 overall numbers declined by around 30%. A European Grassland Butterfly Indicator from 16 European countries shows there has been a 39% decline of grassland butterflies since 1990. The 2010 Red List of European butterflies listed 38 of the 482 European species (8%) as threatened and 44 species (10%) as near threatened (note that 47 species were not assessed). A country level analysis indicates that the average Red List rating is highest in central and mid-Western Europe and lowest in the far north of Europe and around the Mediterranean. The causes of the decline of butterflies are thought to be similar in most countries, mainly habitat loss and degradation and chemical pollution. Climate change is allowing many species to spread northward while bringing new threats to susceptible species. We describe examples of possible conservation solutions and a summary of policy changes needed to conserve butterflies and other insects.

The range of hosts exploited by a parasite is determined by several factors, including host availability, infectivity and exploitability. Each of these can be the target of natural selection on both host and parasite, which will determine the local outcome of interactions, and potentially lead to coevolution. However, geographical variation in host use and specificity has rarely been investigated. Maculinea (= Phengaris ) butterflies are brood parasites of Myrmica ants that are patchily distributed across the Palæarctic and have been studied extensively in Europe. Here, we review the published records of ant host use by the European Maculinea species, as well as providing new host ant records for more than 100 sites across Europe. This comprehensive survey demonstrates that while all but one of the Myrmica species found on Maculinea sites have been recorded as hosts, the most common is often disproportionately highly exploited. Host sharing and host switching are both relatively common, but there is evidence of specialization at many sites, which varies among Maculinea species. We show that most Maculinea display the features expected for coevolution to occur in a geographic mosaic, which has probably allowed these rare butterflies to persist in Europe. This article is part of the theme issue ‘The coevolutionary biology of brood parasitism: from mechanism to pattern’.

Many lycaenid butterfly species have interactions with ants, with 12% obligatorily depending on two sequential sources of larval food, namely host plants and host ants. When host plants are abundant but the density of host ant nests is relatively low, most host plants have no host ant nest in their vicinity and are thus unsuitable for larval survival. Obligatorily myrmecophilous female butterflies, whose caterpillars feed on ant larvae, would have a comparative advantage if they deposit eggs on host plants in the proximity of a host ant nest. However, this ant‐mediated oviposition has been hotly debated. In an open‐air insectory experiment, we tested whether oviposition is ant‐mediated or not for two obligatory myrmecophilous butterfly species, Phengaris (Maculinea) nausithous Bergsträsser and Phengaris teleius Bergsträsser (Lepidoptera: Lycaenidae). Female butterflies could select host plants close to either no ant nest or a nest of one of the two Myrmica species (Hymenoptera: Formicidae) that are thought to be their host ant. Our results support ant‐mediated oviposition in P. teleius, but also indicate that there is no preference for either of the Myrmica species. More eggs were deposited and more caterpillars were found on long flowerheads close to Myrmica ant nests than on those without nests. Our findings suggest that ant presence is more important than flowerhead phenology for females of P. teleius. In contrast, P. nausithous females were not attracted by ants but preferred long flowerheads with a low percentage of green coloration. With these findings, this study contributes to better understanding of the habitat requirements of two highly specialized butterfly species.

The survival of eggs and larvae is dependent on the oviposition site selection of their mothers. In obligate myrmecophilic butterflies, both host plant phenology and host ant presence are expected to affect the decision where to deposit eggs. The importance of ant nest presence in the oviposition site selection of Phengaris butterflies is, however, highly debated. We studied oviposition in the largest Phengaris (Maculinea) alcon population in Portugal, exploiting Gentiana pneumonanthe as the host plant and Myrmica aloba as host ant. We collected phenological plant data and recorded the presence and number of eggs on plants with and without Myrmica ants nearby during the flight period of the butterfly. Females oviposited on tall plants with many tall buds, while the presence of host ant nests weakly affected oviposition on plants where the probability of finding ants at close range was high. Moreover, larger plants with many tall buds close to host ant nests received more eggs. A density‐dependent shift in oviposition was not found as the proportion of buds not infected with eggs did not differ between plants with or without ants, whereas plant characteristics did have an effect. Tall plants with many large buds were associated with earlier oviposition. Our results suggest that females of P. alcon in Portugal choose gentian plants for oviposition mainly based on plant characteristics whereas the vicinity of ants had a weak effect. Moreover, our study shows that testing the ant‐mediated oviposition hypothesis requires baiting ants more than once.