Explaining the sawtooth: latitudinal periodicity in a circadian gene correlates with shifts in generation number

Many temperate insects take advantage of longer growing seasons at lower latitudes by increasing their generation number or voltinism. In some insects, development time abruptly decreases when additional generations are fit into the season. Consequently, latitudinal ‘sawtooth’ clines associated with shifts in voltinism are seen for phenotypes correlated with development time, like body size. However, latitudinal variation in voltinism has not been linked to genetic variation at specific loci. Here, we show a pattern in allele frequency among voltinism ecotypes of the European corn borer moth (Ostrinia nubilalis) that is reminiscent of a sawtooth cline. We characterized 145 autosomal and sex‐linked SNPs and found that period, a circadian gene that is genetically linked to a major QTL determining variation in post‐diapause development time, shows cyclical variation between voltinism ecotypes. Allele frequencies at an unlinked circadian clock gene cryptochrome1 were correlated with period. These results suggest that selection on development time to ‘fit’ complete life cycles into a latitudinally varying growing season produces oscillations in alleles associated with voltinism, primarily through changes at loci underlying the duration of transitions between diapause and other life history phases. Correlations among clock loci suggest possible coupling between the circadian clock and the circannual rhythms for synchronizing seasonal life history. We anticipate that latitudinal oscillations in allele frequency will represent signatures of adaptation to seasonal environments in other insects and may be critical to understanding the ecological and evolutionary consequences of variable environments, including response to global climate change.     

Development, reproduction, voltinism and host synchrony ofMeteorus trachynotus with its hostsChoristoneura fumiferana andC. rosaceana

The form and variability of temperature-dependent development responses were measured for the braconid parasitoidMeteorus trachynotus (Vier.), developing inChoristoneura fumiferana (Clem.) andC. rosaceana (Harr.). It was found that parasitism reduces the duration and variability of postdiapause development inC. rosaceana larvae, and that the development of the parasitoid does not resume until its host emerges from diapause.M. trachynotus development and entry into diapause are controlled by the host. In large, nondiapausing hosts, the parasitoid can complete one generation in about 348 degree-days above 5.9°C. Male and female adults live an average of 22.0 and 23.8 days at 20°C, and the preoviposition period is 1.7 days. Total fecundity averages 194.2 eggs per female and is reduced considerably by low host density. Under our experimental conditions, femaleM. trachynotus lay a maximum of 14.3 eggs per day, with a maximum of 3.7 eggs per host, on average. Simulations based on degree-day accumulation in 13 locations in eastern Canada showed that the parasitoid was well synchronized with its two alternative hosts, thatM. trachynotus could complete three generations in most locations, and that voltinism was essentially determined by entry ofC. rosaceana larvae into diapause. Overlap between adult parasitoids and larvae of the spruce budworm is incomplete, and inadequate synchrony seems to be an important aspect of the ecological interactions between these two organisms.

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Résumé Nous avons mesuré la forme et la variabilité des réactions de cause à effet entre la température et le développement de la braconideMeteorus trachynotus (Vier.) se développant à l'intérieur de larves deChoristoneura fumiferana (Clem.) et deC. rosaceana (Harr.). Le parasitisme réduit la durée et la variabilité de la postdiapause deC. rosaceana, et le développement du parasito?de ne reprend qu'une fois l'h?te émergé de diapause. Le développement et l'entrée en diapause deM. trachynotus sont sous le contr?le de l'h?te. Dans des larves-h?tes agées et non diapausantes, le parasito?de peut engendrer une génération en moins de 348 degrés-jours au-dessus de 5,9°C. Les adultes males et femelles vivent en moyenne 22,0 et 23,8 jours à 20°C, et la période de prèoviposition est de 1,7 jour. La fécondité totale est de 194,2 oeufs par femelle, et une faible densité d'h?tes la réduit considérablement. Dans nos conditions expérimentales, les femelles deM. trachynotus pondent au plus 14,3 oeufs par jour, la moyenne maximale étant de 3,7 oeufs par h?te. Des simulations basées sur l'accumulation de degrés-jours pour 13 endroits dans l'est du Canada ont indiqué que le parasito?de est bien synchronisé avec ses deux h?tes alternants, queM. trachynotus peut engendrer jusqu'à trois générations par année dans la plupart des endroits, et que son voltinisme est déterminé essentiellement par l'entrée en diapause des larves deC. rosaceana. Le chevauchement entre la période de vol des adultes du parasito?de et celle de la disponibilité des larves de la tordeuse des bourgeons de l'épinette est incomplet, et il semble que ce synchronisme inadéquat soit un aspect important dans les interactions écologiques entre ces deux organismes.

     

Effect of predators and host phenology on the maternal and reproductive behaviors ofGargaphia lace bugs (Hemiptera: Tingidae)

Lace bugs of the genus Gargaphia specialize on taxonomically and ecologically diverse host plants. To examine the impact of predation pressure and host phenology on Gargaphia subsocial and reproductive behavior, we compared G. tiliae, a woodland species restricted to riparian trees in the genus Tilia, and G. solani, a specialist on Solanum in early successional habitats. Both lace bug species exhibit maternal care of eggs and nymphs. Predator densities associated with Solanum were higher than those associated with Tilia and were correlated with higher levels of maternal aggression exhibited by G. solani. In both habitats, artificial exclusion of predators significantly increased nymphal survivorship over maternally guarded broods. Both species reduced the costs associated with maternal care by ovipositing into the egg masses of conspecifics. Gargaphia solani and G. tiliae differed most strikingly in voltinism and thus the potential for iteroparity. Leaf age determined the reproductive future of G. tiliae nymphs independent of photoperiod or temperature. Feeding on plants with young foliage was sufficient to trigger oviposition. Constraints imposed by host plants on life-history patterns and maternal options are discussed.     

Summer dormancy ensures univoltinism in the predatory bug Picromerus bidens

The seasonal cycle of Picromerus bidens L. (Heteroptera: Pentatomidae) is usually considered to be univoltine with an obligatory winter egg diapause. Seasonal adaptations of the species were studied in the laboratory and in field experiments. When reared under short-day photoperiodic conditions (L12:D12 and L14:D10), all females began to lay eggs synchronously soon after their emergence. However, in the females reared under long-day conditions (L18:D6 and L20:D4) and outdoors in June–July, oviposition was significantly delayed. This delay in reproduction induced by photoperiodic conditions and then spontaneously terminated was considered to be aestivation. Egg batches laid by females in the laboratory and in the field were kept at 25 °C for two months. From 30.8 to 93.8% of batches contained eggs which hatched without cold treatment between day 14 and 60 after oviposition. The proportion of eggs hatched was 17.7 to 20.9% in the short-day regimes, while it was significantly less (5.7 to 6.0%) under long-day conditions. It is concluded that in some eggs diapause is of low intensity and that if under natural conditions the first batches had been laid at the end of June, nymphs would have hatched at least from some eggs during the same season even without cold treatment. Such untimely hatching would have resulted in the death of nymphs and adults unprepared for overwintering. A photoperiodic response which induces aestivation in the early emerging adults in June–August may prevent early oviposition and occurrence of a second generation and thus maintains univoltinism in P. bidens.     

Changes in life‐history traits of the water strider Aquarius paludum in accordance with global warming

Seasonal records of nymphs of the water strider Aquarius paludum Fabricius (Heteroptera: Gerridae) at a waterway in Kochi prefecture, Japan (33°00′N to 33°30′N), in 2007, show that populations of new generation adults occur four or more times during the year, in mid and late May; late July to early August; September; and October to November. In laboratory experiments, more than 50% of adults are reproductive, irrespective of photoperiod, and this ratio increases to 80% even under a short‐day LD 11.5 : 13.5 h photocycle, which corresponds to the winter season at Kochi (33°N). There is a diminishing photoperiodic response in relation to the induction of diapause compared with measurements made in previous years (1995–1997), suggesting that reproduction may be possible over a much longer period in the near future (and even in winter) if local climate warming is sustained. A high proportion of males sampled in 2008 have small testes and a high proportion of females do not have mature oöcytes even in summer. This contrasts with earlier data showing that the testis volume index for the same period is greater in 1995–1997, and that 75% of females have mature oöcytes. These changes suggest that the Kochi‐Nankoku population of A. paludum is beginning to show partial aestivation. Overwintering adults of both sexes are found to have no mature flight muscles in October/November 2008. This is in marked contrast with earlier data from 1995 and 2004. Adults that are reared in the laboratory also show a lower flight propensity in response to shorter day lengths. The absence of mature flight muscles in the autumn and lower flight propensity under shorter days may indicate a cessation of dispersal between the summer habitats and overwintering sites on land far from the waterways. Taken together, these data suggest that populations of A. paludum in the Kochi‐Nankoku region are continuing to show adaptive changes, apparently in relation to global warming.     

Rising temperature and development in dragonfly populations at different latitudes

1. For modelling the future ecological responses to climate change, data on individual species and on variation within and between populations from different latitudes are required. 2. We examined life cycle regulation and growth responses to temperature in Mediterranean and temperate populations of a widespread European odonate, Orthetrum cancellatum. In an experiment, offspring from individual females from different parts of the range were kept separately to elucidate differences between families. 3. The experiment was run outdoors at 52°N at a natural photoperiod for almost a year. We used four temperature regimes, ambient (i.e. following local air temperature) and ambient temperature increased by 2, 4 and 6 °C, to mimic future temperature rise. A mathematical model was used to categorise the type of seasonal regulation and estimate parameters of the temperature response curve. 4. Growth rate varied significantly with temperature sum, survival and geographic origin, as well as with family. Offspring of all females from the temperate part of the range had a life cycle with a 12 h day‐length threshold necessary to induce diapause (i.e. diapause was induced once day length fell below 12 h). By contrast, Mediterranean families had a 10 h threshold or had an unregulated life cycle allowing winter growth. The temperature response did not significantly differ between populations, but varied between families with a greater variation in the optimum temperature for growth in the Mediterranean population. 5. The variation in seasonal regulation leads to a diversity in voltinism patterns within species, ranging from bivoltine to semivoltine along a latitudinal gradient. Given that the type of seasonal regulation is genetically fixed, rising temperatures will not allow faster than univoltine development in temperate populations. We discuss the consequences of our results in the light of rising temperature in central Europe.     

Global warming affects phenology and voltinism of Lobesia botrana in Spain

• 1 Climate change is promoting alterations of a very diverse nature in the life cycle of an array of insect species, including changes in phenology and voltinism. In Spain, there is observational evidence that the moth Lobesia botrana Den. & Schiff. (Lep.: Tortricidae), a key vine pest that is usually trivoltine in Mediterranean latitudes, tends to advance spring emergence, displaying a partial fourth additional flight, a fact that is potentially attributable to global warming.
• 2 To verify this hypothesis, local temperatures were correlated with L. botrana phenology in six vine‐growing areas of southwestern Spain during the last two decades (1984–2006) by exploiting the database of flight curves obtained with sexual pheromone traps. The dates of second and third flight peaks of the moth were calculated for each area and year and then correlated with both time (years) and local temperatures.
• 3 The results obtained demonstrated a noteworthy trend towards local warming (as a result of global warming) in the last two decades, with mean increases in annual and spring temperatures of 0.9 and 3.0°C, respectively. Therefore, L. botrana phenology has significantly advanced by more than 12 days. Moreover, the phenological advance contributed to increased moth voltinism in 2006 by promoting a complete fourth additional flight, a fact that has never been reported previously to our knowledge in the Iberian Peninsula.
• 4 The potential impact of an earlier phenology and increased voltinism in L. botrana is discussed from an agro‐ecological perspective.

     

Climate change effects on animal ecology: butterflies and moths as a case study

Butterflies and moths (Lepidoptera) are one of the most studied, diverse, and widespread animal groups, making them an ideal model for climate change research. They are a particularly informative model for studying the effects of climate change on species ecology because they are ectotherms that thermoregulate with a suite of physiological, behavioural, and phenotypic traits. While some species have been negatively impacted by climatic disturbances, others have prospered, largely in accordance with their diversity in life-history traits. Here we take advantage of a large repertoire of studies on butterflies and moths to provide a review of the many ways in which climate change is impacting insects, animals, and ecosystems. By studying these climate-based impacts on ecological processes of Lepidoptera, we propose appropriate strategies for species conservation and habitat management broadly across animals.     

Selection for discontinuous life-history traits along a continuous thermal gradient in the butterfly Aricia agestis

Abstract.  1. Voltinism may be conceptualised as the product of development rate and the timing of diapause – two components that together translate gradual environmental variation, through periods of growth and development, into 'generational units'. This may result in very different selection pressures on diapause induction and development time in populations with different numbers of generations per year.
2. Developmental data from univoltine and bivoltine populations of the butterfly Aricia agestis (Lepidoptera: Lycaenidae) in North Wales were used to examine larval development time and the timing of diapause, and their contribution towards voltinism in populations that occur at the same latitude and in geographic proximity to one another along a thermal gradient.
3. The critical photoperiod for diapause induction in univoltines and bivoltines from the same latitude differed by more than 1.5 h.
4. Development time also differed significantly between these populations, in line with predictions that bivoltines would need to exhibit shorter development times in order to achieve two complete generations per year. Shorter development times for bivoltines result in lower pupal weights, suggesting a trade-off exists between generation number and body size that may dictate the position of the transition zone between the two life-history strategies. Analysis of development times in a third population, from southern England, with greater thermal availability than those from North Wales, further supports this hypothesised trade-off.
5. To achieve the conversion of a continuous thermal gradient into the binary biological response from univoltism to bivoltism, bivoltines speed up development, reduce adult body size and shift their diapause induction response.