Dispersal and aggression in a supercolony of the ant Formica pressilabris

Because of their eusociality and diverse adaptations, ants are classic study objects in evolutionary biology. Supercolonies consisting of numerous nests have recently received much attention. Supercoloniality is an ecologically dominant and successful lifestyle, but it may be an evolutionary dead end. A supercolony has extremely many queens, and relatedness between colony members is thus very low. Inclusive fitness theory predicts selfish traits to spread in such low relatedness colonies, and if relatedness is zero, kin selection cannot act on worker traits. In such situations eusociality cannot persist. Dispersal is dangerous to daughter queens, and only a small fraction succeeds in establishing new nests. When relatedness between daughter queens and the rest of a colony is high, kin selection will, however, favor dispersal, because competition against relatives does not benefit daughter queens. But when relatedness is low, daughter queens may maximize their inclusive fitness by staying in their natal colony, although dispersal would be the collective interest of the colony. Non-dispersing by daughter queens is thus selfish behavior and is expected in low relatedness colonies. I studied dispersal between a large nest aggregation and other smaller colonies of the ant Formica pressilabris in Raseborg, Southern Finland. I found a supercolony-like dense aggregation of more than 1 300 nests on a 9 ha large abandoned field, as well as three other nest aggregations a few hundreds of meters away from the assumed supercolony. I studied dispersal between these subpopulations indirectly by estimating gene flow using microsatellite DNA markers. I extracted DNA from 285 nests and studied ten microsatellite loci. In addition to the population genetic study, I performed behavioral experiments, on one hand to determine whether supercolony workers identify intruders at all, and on the other hand to investigate whether the large nest aggregation actually is one supercolony. My results show limited gene flow between the four subpopulations. The two largest subpopulations are viscous, i.e. neighboring nests are genetically more similar to each other than to more distant nests in the same subpopulation. However, my results do not support my hypothesis that supercolony daughter queens disperse less than daughter queens from other colonies in the area. One explanation for this result is that non-dispersal of daughter queens does not show up in microsatellite studies. This might be the case if there is enough male dispersal to even out the gene flow between subpopulations. Another possible explanation is that dispersal is limited from all of the subpopulations, which all seem to be polydomous. Thirdly, it may be that even supercolony daughter queens disperse, which would be against my hypothesis. This possibility is supported by the weakness of the population structuring. These three alternatives are mutually nonexclusive and may all affect my results. In my behavioral experiments I found aggression between nests of the nest aggregation assumed to be a supercolony. Thus, it is not a uniform supercolony, as ants of a colony are by definition not aggressive towards each other. This result is surprising, and such a supercolony-like nest aggregation with aggression between its nests has not been reported earlier. If the nest aggregation actually consists of many smaller polydomous colonies, the result from my population genetic study, which is against my a priori hypothesis, would be expected. My results underline that sufficient attention should be paid to the interactions between individual nests when studying supercolonies.Aitososiaalisuuden ja monimuotoisten sopeumiensa ansiosta muurahaiset ovat klassinen evoluutiobiologian tutkimuskohde. 2000-luvulla lukuisista pesistä koostuvat superkoloniaaliset yhteiskunnat ovat olleet erityisen kiinnostuksen kohteena. Superkoloniaalisuus on ekologisesti menestyksekäs elämänmuoto, mutta se voi olla evolutiivinen umpikuja. Koska superkoloniassa on erittäin paljon lisääntyviä kuningattaria, on sukulaisuus superkoloniassa erittäin alhainen. Alhaisen sukulaisuuden voi sukulaisvalintateorian pohjalta odottaa johtavan itsekkään käyttäytymisen yleistymiseen, ja jos sukulaisuus on nolla, ei luonnonvalinta voi vaikuttaa lisääntymättömien työläisten ominaisuuksiin. Tällaisessa tilanteessa aitososiaalinen elämäntapa ei voi jatkua tai kehittyä. Muurahaisten tytärkuningatarten levittäytyminen on vaarallista, ja vain pieni osa levittäytyjistä onnistuu perustamaan uuden pesän. Kun tytärkuningatarten ja muun yhteiskunnan välinen sukulaisuus on korkea, suosii sukulaisvalinta levittäytymistä, sillä tytärkuningattaren ei kannata jäädä synnyinyhteiskuntaansa kilpailemaan sukulaistensa kanssa. Kun yhteiskunnan sisäinen sukulaisuus on alhainen, voi synnyinpesään jääminen sen sijaan kannattaa, vaikka levittäytyminen olisi yhteiskunnan etu. Tytärkuningatarten levittäytymättömyys on siis itsekästä käyttäytymistä, jonka odotan yleistyvän alhaisen sukulaisuuden yhteiskunnissa. Tutkin kaljuloviniskan (Formica pressilabris) levittäytymistä superkoloniaksi olettamani ison pesäkeskittymän ja sen lähistöltä etsimieni muiden yhteiskuntien välillä Raaseporissa Länsi-Uudellamaalla. Löysin 9 ha:n kokoiselta pellolta yli 1 300 kaljuloviniskan pesää tiheänä, superkoloniamaisena, keskittymänä, ja lisäksi löysin kolme pienempää pesäkeskittymää joidenkin satojen metrien päässä tästä pellosta. Arvioin mikrosatelliitti-DNA:n avulla geenivirran määrää ja täten epäsuorasti levittäytymistä eri osapopulaatioiden välillä. Eristin DNA:ta yhteensä 285 pesästä ja tutkin kymmentä mikrosatelliittilokusta. Lisäksi tein käyttäytymiskokeita selvittääkseni yhtäältä kuinka hyvin superkolonian työläiset tunnistavat vieraita työläisiä ja toisaalta, onko tutkimani pesäkeskittymä ylipäänsä yhtenäinen superkolonia. Tulokseni osoittavat, että geenivirta eri pesäkeskittymien välillä on rajoittunutta. Kahden isoimman osapopulaation sisällä on myös geneettistä viskositeettia, eli lähellä toisiaan sijaitsevat pesät muistuttavat geneettisesti enemmän toisiaan kuin kauempana olevia pesiä. Kuitenkaan tulokseni eivät tue hypoteesiani, että superkolonian tytärkuningattaret levittäytyisivät vähemmän kuin muiden osapopulaatioiden jälkeläiset. Hypoteesini vastainen tulos voi selittyä sillä, että kuningatarten levittäytymättömyys ei näy mikrosatelliitteja analysoitaessa, jos koiraiden levittäytyminen riittää tasoittamaan geenivirtaa osapopulaatioiden välillä. Toinen mahdollinen selitys on, että kaikkien löytämieni yhteiskuntien sukulaisuus on alhainen ja että levittäytyminen on rajoittunutta myös pienemmistä osapopulaatioista. Kolmanneksi voi olla, että superkoloniankin tytärkuningattaret todellisuudessa levittäytyvät siivin ainakin jonkin verran. Tätä vaihtoehtoa tukee löytämäni geneettisen rakenteen heikkous. Kolme vaihtoehtoista selitystä eivät sulje toisiaan pois ja voivat kaikki vaikuttaa tulokseeni. Käyttäytymiskokeissa löysin aggressiota olettamani superkolonian pesien välillä. Kyseessä ei näytä olevan yksi superkolonia, koska yhteiskunnan sisällä ei määritelmän mukaan ole aggressiota. Tulos on aikaisemman tutkimuksen perusteella yllättävä, eikä vastaavaa ulkoisesti superkoloniaaliselta näyttävää pesäkeskittymää, jonka pesien välillä on aggressiota, ole aikaisemmin kuvattu. Jos olettamani superkolonia todellisuudessa on monta pienempää monipesäistä yhteiskuntaa, on myös populaatiogeneettisestä tutkimuksesta saamani tulos odotettu. Käyttäytymiskokeeni tulos korostaa, että tutkittujen superkolonioiden pesien väliset vuorovaikutukset on selvitettävä huolellisesti

Limited dispersal and an unexpected aggression pattern in a native supercolonial ant

Abstract Understanding how social groups function requires studies on how individuals move across the landscape and interact with each other. Ant supercolonies are extreme cooperative units that may consist of thousands of interconnected nests, and their individuals cooperate over large spatial scales. However, the inner structure of suggested supercolonial (or unicolonial) societies has rarely been extensively studied using both genetic and behavioral analyses. We describe a dense supercolony-like aggregation of more than 1,300 nests of the ant Formica (Coptoformica) pressilabris. We performed aggression assays and found that, while aggression levels were generally low, there was some aggression within the assumed supercolony. The occurrence of aggression increased with distance from the focal nest, in accordance with the genetically viscous population structure we observe by using 10 DNA microsatellite markers. However, the aggressive interactions do not follow any clear pattern that would allow specifying colony borders within the area. The genetic data indicate limited gene flow within and away from the supercolony. Our results show that a Formica supercolony is not necessarily a single unit but can be a more fluid mosaic of aggressive and amicable interactions instead, highlighting the need to study internest interactions in detail when describing supercolonies.Peer reviewe

Life history evolution during a climate-driven butterfly range expansion

Climate change pushes species polewards and upwards – as temperatures rise, species move to areas that were previously too cold for them. During range expansions, species encounter unfamiliar environmental conditions, which may require evolutionary adaptation, but expanding populations may often be hampered by their genetic and demographic properties. Whether range-expanding populations can adapt may greatly affect species distributions, but the question is largely unexplored for native species expanding in response to climate change.  In seasonal environments, organisms must endure harsh conditions and synchronise growth and reproduction with the presence of food and mates. To time their life cycles, many animals and plants use seasonal changes in daylength. Insects typically overwinter in diapause (dormancy with paused development and suppressed metabolism), which is induced by short days well before winter. But across-latitude differences in daylength pose challenges for latitudinal range expansions. I focus on whether traits related to seasonal timing and winter survival have evolved during range expansion of the wall brown butterfly (Lasiommata megera) in Sweden. In Chapter I, I confirmed that the wall brown has, in 2000–2020, expanded northwards along the eastern and western coasts of Sweden, and in Chapter II, I demonstrated that these parallel expansions have proceeded independently from the south, in isolation from each other. Laboratory experiments in Chapter I revealed that caterpillars from northern populations have evolved to correctly interpret their local daylength cues. This rapid evolution, repeated along two range expansions, indicates that latitudinal differences in daylength may seldom hinder insect range expansions. In Chapter II, I found that northern range margin populations have lower genetic variation than southern ones but are unlikely to have received much locally maladaptive gene flow from the south. Further, a genomic scan suggested that the parallel phenotypic changes have evolved through non-parallel genetic changes. In Chapter III, a laboratory experiment showed lack of local adaptation to different winters, in contrast to the rapid evolution of diapause timing. Overall winter survival was low in the coldest treatment, indicating that winter temperatures limit the range. In Chapter IV, I studied diapause induction, growth rate, and winter survival in a field setting. Almost all individuals entered diapause, with only minimal impact from the among-population differences found in Chapter I. These evolved differences could stem from natural selection on earlier parts of the generation, which experience longer days than our experiment captured. Further, individuals of northern descent grew faster than those from the south. This could help them grow large enough before winter, yet pre-winter mass did not affect winter survival. This time, natural selection may favour high growth rates in late-hatching individuals with less time to grow before winter. Like in Chapter III, there was no evidence for evolution of improved winter survival, and survival dropped markedly when transplanting individuals outside of the current range. Despite rapid evolution in two traits, cold winters limit the wall brown’s expansion. To predict range expansions, we must pinpoint their drivers, study trait evolution relevant to these drivers, and recognize that traits that are crucial in different seasons may vary in evolvability

Data from: A range-expanding butterfly is susceptible to cold and long winters but shows no signs of local adaptation to winter conditions

Numerous species shift or expand their ranges polewards in response to climate change. Even when expanding species follow their climatic niches, expanding range margin populations are likely to face unfamiliar environmental conditions and thus natural selection for local adaptation. The wall brown butterfly (Lasiommata megera) has expanded northwards in Sweden in the years 2000–2020, most likely as a result of climate change, and has previously been shown to have evolved local adaptations to northern daylength conditions. This evolution has occurred despite hypothesised genetic constraints to adaptation at range margins. We studied local adaptation to winter conditions in four of the previously-studied L. megera populations, using a common garden laboratory experiment with a warm and short, an intermediate, and a cold and long winter treatment. We compared the winter and post-winter survival of caterpillars from two southern core range and two northern range margin populations in Sweden. During the experiment, we measured metabolic rates of a subset of diapausing caterpillars to test whether populations differ in metabolic suppression during diapause. Further, we measured supercooling points, which reflect lower lethal temperature in L. megera, of the same subset of caterpillars. We also compared supercooling points between L. megera and three closely related species with more northern distributions. Few individuals survived the coldest treatment all the way to successful adult emergence, so L. megera seems susceptible to cold winters. Individuals of northern descent did not survive cold winters any better than individuals from southern populations. Similarly, there were no signs of local adaptation in metabolic rates or supercooling points. The comparison among species did not reveal any clear relationship between geographical distribution and supercooling point. Although northern winters probably exert strong selection on L. megera, we provide comprehensive evidence for the lack of local adaptation to winter conditions. This contrasts with the previous finding of quickly-evolved local adaptation in diapause timing, highlighting the need to consider how traits associated with different seasons differ in how they may evolve and facilitate climate change-induced range expansions.Funding provided by: Bolin Centre for Climate Research*Crossref Funder Registry ID: Award Number: Funding provided by: VetenskapsrådetCrossref Funder Registry ID: http://dx.doi.org/10.13039/501100004359Award Number: VR 2017‐04500Funding provided by: VetenskapsrådetCrossref Funder Registry ID: http://dx.doi.org/10.13039/501100004359Award Number: 2017-04159Funding provided by: Carl Tryggers Stiftelse för Vetenskaplig ForskningCrossref Funder Registry ID: http://dx.doi.org/10.13039/501100002805Award Number