Dispersal and life-history traits in a spider with rapid range expansion

Background Dispersal and reproduction are key life-history traits that jointly determine species' potential to expand their distribution, for instance in light of ongoing climate change. These life-history traits are known to be under selection by changing local environmental conditions, but they may also evolve by spatial sorting. While local natural selection and spatial sorting are mainly studied in model organisms, we do not know the degree to which these processes are relevant in the wild, despite their importance to a comprehensive understanding of species' resistance and tolerance to climate change. Methods The wasp spider Argiope bruennichi has undergone a natural range expansion - from the Mediterranean to Northern Europe during the recent decades. Using reciprocal common garden experiments in the laboratory, we studied differences in crucial traits between replicated core (Southern France) and edge (Baltic States) populations. We tested theoretical predictions of enhanced dispersal (ballooning behaviour) and reproductive performance (fecundity and winter survival) at the expansion front due to spatial sorting and local environmental conditions. Results Dispersal rates were not consistently higher at the northern expansion front, but were impacted by the overwintering climatic conditions experienced, such that dispersal was higher when spiderlings had experienced winter conditions as occur in their region. Hatching success and winter survival were lower at the range border. In agreement with theoretical predictions, spiders from the northern leading edge invested more in reproduction for their given body size. Conclusions We found no evidence for spatial sorting leading to higher dispersal in northern range edge populations of A. bruennichi. However, reproductive investment and overwintering survival between core and edge populations differed. These life-history traits that directly affect species' expansion rates seem to have diverged during the recent range expansion of A. bruennichi. We discuss the observed changes with respect to the species' natural history and the ecological drivers associated with range expansion to northern latitudes

Stressresistenz verschiedener Entwicklungsstadien bei Tagfaltern unter dem Einfluss des Klimawandels

Der anthropogene Klimawandel stellt für die Erhaltung der biologischen Vielfalt eine erhebliche Herausforderung dar. Dokumentierte biologische Reaktionen auf den jüngsten Klimawandel beinhalten phänologische und Verbreitungs-Verschiebungen sowie Abnahmen von an Kälte angepassten und Zunahmen von an Wärme angepassten Arten. Letzteres zeigt, dass einige Arten unter den sich ändernden Bedingungen leiden werden, während andere davon profitieren können. Welche spezifischen biologischen Eigenschaften darüber bestimmen, ob eine bestimmte Art ein „Gewinnen“ oder „Verlierer“ des Klimawandels sein wird, ist bis jetzt jedoch weitgehend unbekannt. Diese Dissertation untersuchte im ersten Experiment bei dem tropischen Schmetterling Bicyclus anynana welches Entwicklungsstadium am empfindlichsten auf Hitzestress reagiert. Ich konnte zeigen, dass Entwicklungsstadien deutlich in ihrer Hitzetoleranz variierten und Eier die höchste Anfälligkeit gegenüber Hitze zeigten. Auffällig war, dass die meisten Veränderungen in der Hitzetoleranz durch Unterschiede in der Körpermasse erklärt werden konnten, was somit zukünftig Einschränkungen in der Anpassungsfähigkeit mit sich bringen könnte. Ich schließe daraus, dass das Überleben der Arten unter dem Einfluss des Klimawandels vermutlich von anderen als dem auffälligen Imaginalstadium abhängt. Im zweiten Experiment habe ich die Stresstoleranz (Hitze und Trockenheit) während der frühen Entwicklung, bei drei verwandten Schmetterlingsarten mit unterschiedlichen Anfälligkeiten gegenüber dem Klimawandel, untersucht. Diese Arten sind Lycaena tityrus, L. dispar und L. helle. Die am meisten gefährdete Art (L. helle) zeigte den stärksten Rückgang des Schlupferfolges unter Hitze- und Trockenstress. Ich konnte darlegen, dass die Stresstoleranz während der frühen Entwicklung von entscheidender Bedeutung für das Überleben der Arten unter dem Einfluss des Klimawandels sein kann. Das dritte Experiment untersuchte die Reaktionen auf simulierte Hitzewellen während der Larven- und Puppenentwicklung und die daraus resultierenden Fitnessimplikationen für Lycaena tityrus, L. dispar und L. helle. Obwohl sich die Arten signifikant in ihren Reaktionen in den Versuchsgruppen unterschieden, scheint eine solche Variation weitgehend durch Selektionsdrücke, die mit den spezifischen Entwicklungswegen assoziiert sind, bestimmt zu sein. Ich fand heraus, dass die simulierten Hitzewellen nur geringe Auswirkungen auf Fitness-Komponenten, einschließlich des Fettgehalts und der Immunfunktion, hatten. Folglich scheinen alle drei Arten in der Lage zu sein, mit den projizierten Veränderungen während ihrer Larven- und Puppenentwicklung zurechtzukommen. Studie 4 verglich die Plastizität in der Stresstoleranz im adulten Stadium in diesen drei Feuerfalterarten. Die phänotypische Plastizität ist die erste Verteidigungslinie gegen Umweltveränderungen und kann für das Überleben von Arten unter dem Einfluss des Klimawandels von großer Bedeutung sein. Im Gegensatz zu meinen Vorhersagen zeigten die drei untersuchten Arten keine ausgeprägte Variation der Stressresistenz, obwohl sich die plastischen Kapazitäten in der Temperaturstressresistenz unterschieden. Insgesamt schienen meine Ergebnisse eher die Populations- als die Art-spezifischen Muster wiederzugeben. Experiment 5 untersuchte mögliche Unterschiede in den direkten und indirekten Entwicklungswegen von L. tityrus. Wie im vierten Experiment fand ich dabei keinen Hinweis auf negative Auswirkungen erhöhter Temperaturen und Hitzewellen. Darüber hinaus unterschieden sich die Muster nicht zwischen sich direkt und vermutlich mehr zeitlich beschränkten sich indirekt entwickelnden Individuen. Ich vermute, dass Art-spezifische Eigenschaften wichtiger sein könnten als potenzielle zeitliche Beschränkungen. Die letzte Studie wurde durchgeführt, um die Auswirkungen der veränderten Winterbedingungen auf das Überleben von L. tityrus zu testen. Ich fand heraus, dass wärmere und feuchtere Winterbedingungen die Überlebensraten deutlich verminderten. Diese negativen Auswirkungen beschränkten sich jedoch auf das Überleben während der Diapause und hatten keinen messbaren Effekt für die spätere individuelle Fitness der Falter. Ich gehe davon aus, dass die Überwinterung ein wichtiger Faktor für die Anfälligkeit gegenüber dem Klimawandel ist. Um das Schicksal bestimmter Arten und Populationen unter dem voranschreitenden Klimawandel vorherzusagen, müssen zwingend mehr Daten zur Stresstoleranz in verschiedenen Entwicklungsstadien, aus einem möglichst breiten Spektrum von Arten, zusammengetragen werden.Anthropogenic climate change may pose substantial challenges to biodiversity conservation. Well-documented biological responses to recent climate change include phenological and range shifts as well as declines in cold-adapted but increases in warm-adapted species. The latter shows that some species will suffer while others will benefit from ongoing changes. However, the specific biological features determining whether a given species is becoming a ‘winner’ or ‘loser’ of climate change are hitherto largely unknown. This doctoral thesis investigated in the first experiment which life stage is the most sensitive one with regard to heat stress in the tropical butterfly Bicyclus anynana. I found that developmental stages clearly differed in heat tolerance, which was lowest in eggs. Strikingly, most of the variation found in thermal tolerance was explained by differences in body mass, which may thus impose a severe constraint on adaptive variation in stress tolerance. I conclude that species survival under climate change is more dependent on other than the typically most conspicuous adult stage. In the second experiment, I compared three related butterfly species of different vulnerability to climate change in their stress tolerance (heat and drought) during early development. These species are Lycaena tityrus, L. dispar and L. helle. The arguably most vulnerable species (L. helle) showed the strongest decline in egg hatching success under heat and desiccation stress. I showed that stress tolerance during early development may be of key importance for species survival under climate change. The third experiment tested the responses to simulated heat waves during larval and pupal development and the resulting fitness implications in Lycaena tityrus, L. dispar and L. helle. Although species differed significantly in their responses to treatments, such variation appears to be largely ruled by selection pressures associated with the specific developmental pathway. I found that the simulated heat waves had only little effect on fitness components including fat content and immune function. Consequently, all three species appear to be capable of dealing with projected changes during their larval and pupal development. Study 4 compared plasticity in stress tolerance in the adult life stage in these three Copper butterfly species. Phenotypic plasticity often comprises the first line of defense against environmental change and may be of utmost importance for survival under climate change. Contrary to my predictions, species did not show pronounced variation in stress resistance, though plastic capacities in temperature stress resistance did vary across species. Overall, my results seemed to reflect population- rather than species-specific patterns. Study 5 investigated possible differences in direct and indirect developing individuals of L. tityrus. I found no evidence for detrimental effects of increased temperatures and even simulated heat waves as in the fourth experiment. Besides that, the patterns did not differ between directly and putatively more time constrained indirectly developing individuals. I suggest that species attributes may be more important than potential time constraints imposed by different developmental pathways. The final study was conducted to test for the impact of changing winter conditions on the survival of L. tityrus. I found that warmer and moister winter conditions substantially decreased survival rates. But these detrimental effects were restricted to diapause survival and had no measurable effect on subsequent performance. I suggest that overwintering survival is an important determinant of vulnerability to climate change. Collating more data on stress tolerance in different life stages from a broader range of species will be of crucial importance for enhancing our abilities to predict the fate of particular species and populations under ongoing climate change

Data from: Effects of temperature and drought on early life stages in three species of butterflies: mortality of early life stages as a key determinant of vulnerability to climate change?

Anthropogenic climate change poses substantial challenges to biodiversity conservation. Well-documented responses include phenological and range shifts, and declines in cold but increases in warm-adapted species. Thus, some species will suffer while others will benefit from ongoing change, although the biological features determining the prospects of a given species under climate change are largely unknown. By comparing three related butterfly species of different vulnerability to climate change, we show that stress tolerance during early development may be of key importance. The arguably most vulnerable species showed the strongest decline in egg hatching success under heat and desiccation stress, and similar pattern also for hatchling mortality. Research, especially on insects, is often focussed on the adult stage only. Thus, collating more data on stress tolerance in different life stages will be of crucial importance for enhancing our abilities to predict the fate of particular species and populations under ongoing climate change

raw Data

These is the complete raw data file for survival rates of eggs and hatchlings under control, heat and desiccation/food stress treatment

Data from: Carried over: heat stress in the egg stage reduces subsequent performance in a butterfly

Increasing heat stress caused by anthropogenic climate change may pose a substantial challenge to biodiversity due to associated detrimental effects on survival and reproduction. Therefore, heat tolerance has recently received substantial attention, but its variation throughout ontogeny and effects carried over from one developmental stage to another remained largely neglected. To explore to what extent stress experienced early in life affects later life stages, we here investigate effects of heat stress experienced in the egg stage throughout ontogeny in the tropical butterfly Bicyclus anynana. We found that detrimental effects of heat stress in the egg stage were detectable in hatchlings, larvae and even resulting adults, as evidenced by decreased survival, growth, and body mass. This study shows that even in holometabalous insects with discrete life stages effects of stress experienced early in life are carried over to later stages, substantially reducing subsequent fitness. We argue that such effects need to be considered when trying to forecast species responses to climate change

raw_data

The data file consists of the data for egg survival, hatchling survival, head capsule width, pupation/eclosion rate and adult heat survival with body mass

Results of general linear models (GLMs) for the effects of (a) egg temperature on egg survival rate, (b) egg temperature and larval heat stress on hatchling survival rate, (c) egg temperature, larval heat stress and survival (dead versus alive individuals) on head capsule width of hatchlings, and for the effects of egg temperature on the survival rate during (d) the larval and (e) the pupal stage in <i>Bicyclus anynana</i>.

<p>Significant <i>P</i>-values are given in bold.</p

Results of a nominal logistic regression for the effects of egg temperature (fixed), cage (nested within temperature; random), sex (fixed), adult body mass, thorax-abdomen ratio and abdomen fat content (covariates) on adult heat survival in <i>Bicyclus anynana</i>.

<p>Significant <i>P</i>-values are given in bold.</p

Schematic figure of the experimental design used.

<p>Eggs collected from stock population females were randomly divided and exposed to six temperatures for 24 hours each. Thereafter, one day-old hatchlings were exposed to either 27°C or 37°C, after which survival and head capsule width were measured. Another cohort of resulting hatchlings was reared under control conditions until adult eclosion and then exposed for 24 h to 37°C, after which heat survival and other traits were scored.</p

Results of general linear mixed models (GLMMs) for the effects of egg temperature (fixed), cage (nested within temperature; random), and sex (fixed) on (a) adult body mass, (b) thorax-abdomen ratio, and (c) abdomen fat content in <i>Bicyclus anynana</i>.

<p>Significant <i>P</i>-values are given in bold.</p