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The evolutionary ecology of niche separation: Studies on the sympatric butterflies Leptidea sinapis and Leptidea reali
Stockholm University, Faculty of Science, Department of Zoology.
2009 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Studies of ecology and evolution have become largely integrated, and increasing attention is paid to the role of ecology for speciation and post speciation divergence. In this thesis I have applied an in-depth approach studying the ecology of a butterfly species pair; the morphologically virtually identical sister-species, the Wood white (Leptidea sinapis) and Reál’s wood white (Leptidea reali). PAPER I showed a quite deep between-species division in sequence data from mitochondrial DNA. The reuniting in secondary contact zones might in contrast be quite recent, as males of L. sinapis and L. reali cannot distinguish between con- and heterospecific females (PAPER II) and since the between-species niche separation is incomplete (PAPER III, IV, V). Furthermore, the two species have partitioned their niches in different directions in different European regions as the two species shift habitat generalist and specialist roles throughout their joint distribution (PAPER III). However, the local niche partitioning has resulted in species-specific adaptations in terms of propensity to enter diapause (PAPER III, V, VI), host plant acceptance (PAPER V), and in ability to use host plant as cue for the decision to enter diapause or direct development (PAPER VI). The habitat separation is decoupled from host plant preference, at least in south central Sweden (PAPER IV), which implies that selection for niche partitioning has acted on habitat preferences directly and not via divergent selection on host plant preference. Finally, there is a high cost of appearing at a site where the other species is in the majority as much time (PAPER VII) and energy (PAPER II) are devoted to court heterospecific females or being courted by heterospecific males (PAPER VII). Hence, selection likely favours habitat specialisation in the rarest species in each region, and the direction of niche separation might simply be decided by which species that reached an area first. The species that first colonises an area would then most likely become a generalist filling up all suitable habitats, whereas the second invader might be forced to specialise, as the cost of being rare is too large everywhere but in the core population. This thesis highlights the role of ecology, and especially of local processes, for post-speciation selection and character displacement.

 

Place, publisher, year, edition, pages
Stockholm: Department of Zoology, Stockholm University , 2009. , 44 p.
Keyword [en]
Lepidoptera, ecological character displacement, reproductive isolation, species discrimination, habitat, host plant, life history, sexual selection, female choice
National Category
Biological Sciences
Research subject
Animal Ecology
Identifiers
URN: urn:nbn:se:su:diva-30822ISBN: 978-91-7155-964-7 (print)OAI: oai:DiVA.org:su-30822DiVA: diva2:274287
Public defence
2009-11-27, Magnélisalen, Kemiska övningslaboratoriet, Svante Arrhenius väg 16 B, Stockholm, 10:00 (English)
Opponent
Supervisors
Note
At the time of the doctoral defense, the folowing papers were unpublished and had a status as follows: Paper 1:Manuscript. Paper 6:Manuscript. Paper 7:ManuscriptAvailable from: 2009-11-05 Created: 2009-10-27 Last updated: 2014-10-13Bibliographically approved
List of papers
1. Genetic differentiation and phylogeographic patterns in European populations of Leptidea sinapis and L. reali
Open this publication in new window or tab >>Genetic differentiation and phylogeographic patterns in European populations of Leptidea sinapis and L. reali
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(English)Manuscript (preprint) (Refereed)
Abstract [en]

The direction of a coevolutionary interaction can differ between local populations as in the butterflies Leptidea sinapis and L. reali. The morphologically virtually identical sister-species have partitioned their niches differently in different parts of their distribution by shifting habitat specialist and generalist roles between different sympatric areas. Hence, a species that is a generalist in some areas can be a local specialist in others, and vice versa. We have sequenced the mitochondrial COI gene from specimens collected across Europe in order to (i) describe the between-species variation over a large area, (ii) identify possible glacial refugia and re-colonisation routes to obtain a phylogeographic hypothesis for explaining the geographic mosaic of niche separation and (iii) apply a population genetic approach to determine the level of intraspecific genetic differentiation. The results show evidence for species distinctiveness throughout Europe. Only small variation was found in L. reali, whereas the haplotype network of L. sinapis showed a deep division into two haplotype families of which one was restricted to Spain and the other was widespread over the continent (including Spain). The widespread haplotype family was divided into two common variants, one eastern and one western, each being surrounded by rare haplotypes. The both deep and shallow genetic differentiation implies that L. sinapis might have been divided into different refugia during several glaciations. Both species showed significant genetic differentiation in pairwise ФST, and as habitat generalist populations could differ significantly from other habitat generalist populations but not from habitat specialist populations, we conclude that this study supports that the geographic mosaic of niche separation is caused by local processes rather than common ancestry of local habitat generalists or specialists within each species

Keyword
Lepidoptera, Pieridae: Leptidea; COI; mitochondrial DNA, niche separation, glacial refugia, starlike pattern, geographic mosaic, ФST
National Category
Biological Sciences
Identifiers
urn:nbn:se:su:diva-30789 (URN)
Available from: 2009-10-27 Created: 2009-10-27 Last updated: 2014-10-13
2. Female mate choice determines reproductive isolation between sympatric butterflies
Open this publication in new window or tab >>Female mate choice determines reproductive isolation between sympatric butterflies
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2008 (English)In: Behavioral Ecology and Sociobiology, Vol. 62, 873-886 p.Article in journal (Refereed) Published
Place, publisher, year, edition, pages
Berlin: Springer, 2008
Identifiers
urn:nbn:se:su:diva-22033 (URN)doi:10.1007/s00265-007-0511-2 (DOI)000254177600002 ()
Available from: 2007-12-19 Created: 2007-12-19 Last updated: 2014-10-13Bibliographically approved
3. Niche separation in space and time between two sympatric sister species—a case of ecological pleiotropy
Open this publication in new window or tab >>Niche separation in space and time between two sympatric sister species—a case of ecological pleiotropy
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2008 (English)In: Evolutionary Ecology, ISSN 0269-7653Article in journal (Refereed) Published
Abstract [en]

Abstract We investigate the niche separation in space and time between the Palearctic sister species Leptidea sinapis and L. reali (Lepidoptera, Pieridae) in central Sweden. Using field sampling, we show that L. reali is a habitat specialist confined to meadows, whereas L. sinapis is a habitat generalist also inhabiting forests. This difference in habitat utilization was corroborated by experimental release of laboratory-reared L. sinapis and L. reali in two adjacent forest and meadow habitats during their natural flight period; virtually all recaptured L. reali that were released in the forest were later caught in the meadow, whereas L. sinapis shifted equally often from meadow to forest as in the opposite direction. In the field, both species fly in May–June, but L. reali appears on average a week earlier in spring and has a substantial second generation in July, whereas L. sinapis is practically univoltine. When overwintered pupae were incubated under identical conditions in the laboratory, females did, however, not differ in phenology, and L. sinapis males actually emerged earlier than L. reali males. When larvae were reared at 23°C on the host plant Lotus corniculatus at a range of daylengths, both species produced a substantial proportion of directly developing individuals at an 18.5 h daylength or longer. When reared at 23°C and a 22 h daylength, L. reali showed an overall higher propensity to develop directly than L. sinapis on plant species originating from both the meadow and the forest habitat. Both Leptidea species showed a lower propensity to enter direct development on forest associated plants than on meadow associated plants. Hence, we suggest that the difference in phenology and voltinism between L. sinapis and L. reali is largely the result of environmentally implemented ecological pleiotropic effects caused by the between-species difference in habitat preference.

Keyword
Temporal and spatial niche-partitioning, Geographic mosaic, Secondary contact, Diapause, Direct development, Host plants
National Category
Ecology
Identifiers
urn:nbn:se:su:diva-20928 (URN)doi:10.1007/s10682-007-9155-y (DOI)000251651100001 ()
Available from: 2008-02-13 Created: 2008-02-13 Last updated: 2014-10-13Bibliographically approved
4. Habitat choice precedes host plant choice - niche separation in a species pair of a generalist and a specialist butterfly
Open this publication in new window or tab >>Habitat choice precedes host plant choice - niche separation in a species pair of a generalist and a specialist butterfly
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2008 (English)In: Oikos, Vol. 117, no 9, 1337-1344 p.Article in journal (Refereed) Published
Abstract [en]

The sister species Leptidea reali and L. sinapis have partitioned their niches differently in different parts of their sympatric distribution. In Spain and France L. sinapis is a widespread generalist whereas L. reali is specialized on high altitude open areas. Interestingly, the reverse is true in Ireland and the Czech Republic where L. reali is widespread and L. sinapis specialized on meadows. In Sweden, L. reali is a habitat specialist confined to meadows, whereas L. sinapis is a habitat generalist also inhabiting forests. Ultimately, the geographic mosaic of niche separation is the result of local processes in each contact zone or a secondary effect of the host plant distribution, if L. sinapis and L. reali prefer different legume host plants. Hence, in Sweden L. sinapis might utilize the forest habitat either due to a wider habitat preference or due to a wider host plant preference than L. reali. Studies of wild butterflies showed that L. sinapis laid 26% of their eggs on forest-associated legumes compared to 6% in L. reali, although laboratory experiments showed that both species had virtually identical host plant preferences strongly preferring the meadow-associated legume Lathyrus pratensis. Furthermore, flight duration tests in a variety of temperatures demonstrated a between-species difference; L. sinapis females reached their flight optimum at a lower temperature than L. reali females. The lower L. sinapis flight temperature optimum is most probably a secondary effect due to habitat-specific selection, and therefore a consequence rather than the cause of the habitat partitioning. The finding that habitat choice precedes host plant choice suggests that the European geographic mosaic of niche separation, with L. sinapis and L. reali shifting habitat specialist/generalist roles, is not caused by rigid between-species differences in a related niche parameter, but instead is a result of local processes within each secondary contact zone.

Place, publisher, year, edition, pages
Lund: Department of Ecology, Lund university, 2008
Identifiers
urn:nbn:se:su:diva-22034 (URN)000258410200007 ()
Available from: 2008-12-11 Created: 2008-12-11 Last updated: 2014-10-28Bibliographically approved
5. Host plant preference and performance of the sibling species of butterflies Leptidea sinapis and Leptidea reali: a test of the trade-off hypothesis for food specialisation.
Open this publication in new window or tab >>Host plant preference and performance of the sibling species of butterflies Leptidea sinapis and Leptidea reali: a test of the trade-off hypothesis for food specialisation.
2009 (English)In: Oecologia, ISSN 0029-8549, Vol. 159, no 1, 127-137 p.Article in journal (Refereed) Published
Abstract [en]

A large proportion of phytophagous insect species are specialised on one or a few host plants, and female host plant preference is predicted to be tightly linked to high larval survival and performance on the preferred plant(s). Specialisation is likely favoured by selection under stable circumstances, since different host plant species are likely to differ in suitability-a pattern usually explained by the "trade-off hypothesis", which posits that increased performance on a given plant comes at a cost of decreased performance on other plants. Host plant specialisation is also ascribed an important role in host shift speciation, where different incipient species specialise on different host plants. Hence, it is important to determine the role of host plants when studying species divergence and niche partitioning between closely related species, such as the butterfly species pair Leptidea sinapis and Leptidea reali. In Sweden, Leptidea sinapis is a habitat generalist, appearing in both forests and meadows, whereas Leptidea reali is specialised on meadows. Here, we study the female preference and larval survival and performance in terms of growth rate, pupal weight and development time on the seven most-utilised host plants. Both species showed similar host plant rank orders, and larvae survived and performed equally well on most plants with the exceptions of two rarely utilised forest plants. We therefore conclude that differences in preference or performance on plants from the two habitats do not drive, or maintain, niche separation, and we argue that the results of this study do not support the trade-off hypothesis for host plant specialisation, since the host plant generalist Leptidea sinapis survived and performed as well on the most preferred meadow host plant Lathyrus pratensis as did Leptidea reali although the generalist species also includes other plants in its host range.

Place, publisher, year, edition, pages
Berlin: Springer, 2009
Identifiers
urn:nbn:se:su:diva-15953 (URN)10.1007/s00442-008-1206-8 (DOI)000262576700012 ()19002503 (PubMedID)
Available from: 2009-02-06 Created: 2009-02-06 Last updated: 2014-10-13Bibliographically approved
6. Host plant induced larval decision-making in a habitat/host plant generalist butterfly
Open this publication in new window or tab >>Host plant induced larval decision-making in a habitat/host plant generalist butterfly
2010 (English)In: Ecology, ISSN 0012-9658, E-ISSN 1939-9170, Vol. 91, 15-21 p.Article in journal (Refereed) Published
Abstract [en]

Phenotypic plasticity can be a passive response to fluctuating environmental conditions or an active and presumably adaptive (evolved) response selected for in different environments. Here we ask if the larval decision to enter diapause when reared on a host plant associated with a colder habitat is an active or a passive response to host plant quality or suitability. We compare plasticity in larval propensity to enter diapause of the habitat generalist butterfly Leptidea sinapis and the meadow specialist Leptidea reali in a range of temperatures and long daylength on a forest plant, Lathyrus linifolius, and a meadow-associated plant, Lathyrus pratensis. The warmer meadow habitat promotes direct development whereas the colder forest habitat is conducive to diapause. Larvae of L. sinapis had a higher propensity to enter diapause when reared on the forest plant L. linifolius across all temperatures. Conversely, the propensity of L. reali to enter diapause was consistently lower and did not differ between host plants. Larval growth rates were similar between and within butterfly species and between host plants. Hence, we conclude that larval pathway decision-making in L. sinapis is an active response mediated by information from their host plants.

Keyword
Habitat, host plant, generalist, specialist, phenotypic plasticity, adaptation, Lepidoptera: Leptidea, polyspecialist, growth rate, development, life history, Lathyrus
Identifiers
urn:nbn:se:su:diva-30791 (URN)10.1890/09-0328.1 (DOI)
Funder
Swedish Research Council
Available from: 2009-10-27 Created: 2009-10-27 Last updated: 2017-12-12Bibliographically approved
7. Heterospecific courtships, Allee-effects and niche separation between Leptidea sinapis and Leptidea reali
Open this publication in new window or tab >>Heterospecific courtships, Allee-effects and niche separation between Leptidea sinapis and Leptidea reali
(English)Manuscript (preprint) (Other (popular science, discussion, etc.))
Abstract [en]

Increasing attention is given to coevolutionary studies and to the role of ecology in local adaptation. The coevolutionary process can act in parallel throughout the distribution of species that interact in similar ecologies, whereas species interacting in varied ecological conditions might coevolve in different directions in different local populations. The butterflies Leptidea sinapis and L. reali have partitioned their niches differently in different parts of their sympatric distribution, with one species being a local habitat generalist in several different regions, and a local specialist in other areas where the sister species has adopted the habitat generalist role. Niche separation is likely independent of resource competition in this phytophagous system, and we study the potential for heterospecific sexual interference competition to redefine the suitability of a habitat and select for niche separation. We used the average female mating success in large outdoor cage experiments that varied both the absolute and relative density of the two species to estimate potential fitness costs of being in local minority. The mating success was unaffected by absolute density (conspecifics/m2) but strongly affected by the proportion of con- and heterospecifics in each cage. The proportion of mated females was ten times higher when a conspecific couple spent the day alone in the cage compared to when the single couple shared the cage with five heterospecific pairs. Being in the minority thus resulted in strong sexual interference from the locally more common competitor. We propose that these Allee effects select for habitat specialisation in the locally rare species as individuals leaving the core population likely suffer decreased fitness from spending time in heterospecific courtship. Hence, habitat suitability might depend less on local resource availability and more on the presence or absence of a local sexual competitor in this system.

Keyword
Lepidoptera: Pieridae; sexual interference; male harassment; geographic mosaic; coevolution; mating success; source-sink; local adaptation; character displacement
Identifiers
urn:nbn:se:su:diva-30792 (URN)
Available from: 2009-10-27 Created: 2009-10-27 Last updated: 2014-10-13

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