Christina M. Holzapfel

Genetic shift in photoperiodic response correlated with global warming

To date, all altered patterns of seasonal interactions observed in insects, birds, amphibians, and plants associated with global warming during the latter half of the 20th century are explicable as variable expressions of plastic phenotypes. Over the last 30 years, the genetically controlled photoperiodic response of the pitcher-plant mosquito, Wyeomyia smithii, has shifted toward shorter, more southern daylengths as growing seasons have become longer. This shift is detectable over a time interval as short as 5 years. Faster evolutionary response has occurred in northern populations where selection is stronger and genetic variation is greater than in southern populations. W. smithii represents an example of actual genetic differentiation of a seasonality trait that is consistent with an adaptive evolutionary response to recent global warming.

Resolving postglacial phylogeography using high-throughput sequencing

The distinction between model and nonmodel organisms is becoming increasingly blurred. High-throughput, second-generation sequencing approaches are being applied to organisms based on their interesting ecological, physiological, developmental, or evolutionary properties and not on the depth of genetic information available for them. Here, we illustrate this point using a low-cost, efficient technique to determine the fine-scale phylogenetic relationships among recently diverged populations in a species. This application of restriction site-associated DNA tags (RAD tags) reveals previously unresolved genetic structure and direction of evolution in the pitcher plant mosquito, Wyeomyia smithii, from a southern Appalachian Mountain refugium following recession of the Laurentide Ice Sheet at 22,000–19,000 B.P. The RAD tag method can be used to identify detailed patterns of phylogeography in any organism regardless of existing genomic data, and, more broadly, to identify incipient speciation and genome-wide variation in natural populations in general.

Genetic response to rapid climate change: it's seasonal timing that matters.

The primary nonbiological result of recent rapid climate change is warming winter temperatures, particularly at northern latitudes, leading to longer growing seasons and new seasonal exigencies and opportunities. Biological responses reflect selection due to the earlier arrival of spring, the later arrival of fall, or the increasing length of the growing season. Animals from rotifers to rodents use the high reliability of day length to time the seasonal transitions in their life histories that are crucial to fitness in temperate and polar environments: when to begin developing in the spring, when to reproduce, when to enter dormancy or when to migrate, thereby exploiting favourable temperatures and avoiding unfavourable temperatures. In documented cases of evolutionary (genetic) response to recent, rapid climate change, the role of day length (photoperiodism) ranges from causal to inhibitory; in no case has there been demonstrated a genetic shift in thermal optima or thermal tolerance. More effort should be made to explore the role of photoperiodism in genetic responses to climate change and to rule out the role of photoperiod in the timing of seasonal life histories before thermal adaptation is assumed to be the major evolutionary response to climate change.

Adaptation to temperate climates

Abstract Only model organisms live in a world of endless summer. Fitness at temperate latitudes reflects the ability of organisms in nature to exploit the favorable season, to mitigate the effects of the unfavorable season, and to make the timely switch from one life style to the other. Herein, we define fitness as Ry, the year‐long cohort replacement rate across all four seasons, of the mosquito, Wyeomyia smithii, reared in its natural microhabitat in processor‐controlled environment rooms. First, we exposed cohorts of W. smithii, from southern, midlatitude, and northern populations (30–50°N) to southern and northern thermal years during which we factored out evolved differences in photoperiodic response. We found clear evidence of evolved differences in heat and cold tolerance among populations. Relative cold tolerance of northern populations became apparent when populations were stressed to the brink of extinction; relative heat tolerance of southern populations became apparent when the adverse effects of heat could accumulate over several generations. Second, we exposed southern, midlatitude, and northern populations to natural, midlatitude day lengths in a thermally benign midlatitude thermal year. We found that evolved differences in photoperiodic response (1) prevented the timely entry of southern populations into diapause resulting in a 74% decline in fitness, and (2) forced northern populations to endure a warm‐season diapause resulting in an 88% decline in fitness. We argue that reciprocal transplants across latitudes in nature always confound the effects of the thermal and photic environment on fitness. Yet, to our knowledge, no one has previously held the thermal year constant while varying the photic year. This distinction is crucial in evaluating the potential impact of climate change. Because global warming in the Northern Hemisphere is proceeding faster at northern than at southern latitudes and because this change represents an amelioration of the thermal environment and a concomitant increase in the duration of the growing season, we conclude that there should be more rapid evolution of photoperiodic response than of thermal tolerance as a consequence of global warming among northern, temperate ectotherms.

Light, Time, and the Physiology of Biotic Response to Rapid Climate Change in Animals

Examination of temperate and polar regions of Earth shows that the nonbiological world is exquisitely sensitive to the direct effects of temperature, whereas the biological world is largely organized by light. Herein, we discuss the use of day length by animals at physiological and genetic levels, beginning with a comparative experimental study that shows the preeminent role of light in determining fitness in seasonal environments. Typically, at seasonally appropriate times, light initiates a cascade of physiological events mediating the input and interpretation of day length to the output of specific hormones that ultimately determine whether animals prepare to develop, reproduce, hibernate, enter dormancy, or migrate. The mechanisms that form the basis of seasonal time keeping and their adjustment during climate change are reviewed at the physiological and genetic levels. Future avenues for research are proposed that span basic questions from how animals transition from dependency on tropical cues to temperate cues during range expansions, to more applied questions of species survival and conservation biology during periods of climatic stress.

Complications of complexity: integrating environmental, genetic and hormonal control of insect diapause

Understanding gene interaction and pleiotropy are long-standing goals of developmental and evolutionary biology. We examine the genetic control of diapause in insects and show how the failure to recognize the difference between modular and gene pleiotropy has confounded our understanding of the genetic basis of this important phenotype. This has led to complications in understanding the role of the circadian clock in the control of diapause in Drosophila and other insects. We emphasize three successive modules - each containing functionally related genes - that lead to diapause: photoperiodism, hormonal events and diapause itself. Understanding the genetic basis for environmental control of diapause has wider implications for evolutionary response to rapid climate change and for the opportunity to observe evolutionary change in contemporary time.

Predator-mediated, non-equilibrium coexistence of tree-hole mosquitoes in southeastern North America

SummaryMosquito populations in tree holes in northern Florida (30.6° N lat.), USA are held below their carrying capacities by a self-limiting, cannabalistic predator. Within tree holes, extinctions and reinvasions are common; in the system as a whole, extinctions and immigrations occur without regard to community composition, tree-hole size or stability, or average number of species present. Little, if any, density-dependent development takes place. There is no evidence that the community ever reaches equilibrium, that competition is taking place, or that competition has been an important factor structuring this mosquito community. Rather, examination of related species in the same genera suggests that the principal determinants of their coexistence relate to the adaptations already possessed by each species at the time of their first encounter. Thus, unless experimentally demonstrated or reasonably inferred from circumstantial evidence, competition and coevolved niche shifts cannot be invoked to explain the coexistence of a diversity of species within a habitat type, no matter how circumscribed or discrete that habitat.

EVOLUTION OF THE GENETIC ARCHITECTURE UNDERLYING FITNESS IN THE PITCHER-PLANT MOSQUITO, WYEOMYIA SMITHII

We examined the genetic basis for evolutionary divergence among geographic populations of the pitcher‐plant mosquito, Wyeomyia smithii, using protein electrophoresis and line‐cross analysis. Line‐cross experiments were performed under both low density, near‐optimal conditions, and at high, limiting larval densities sufficient to reduce fitness (rc) in parental populations by approximately 50%. We found high levels of electrophoretic divergence between ancestral and derived populations, but low levels of divergence between two ancestral populations and between two derived populations. Assessed under near‐optimal conditions, the genetic divergence of fitness (rc) between ancestral and derived populations, but not between two derived populations or between two ancestral populations, has involved both allelic (dominance) and genic (epistatic) interactions. The role of dominance and epistasis in the divergence of rc among populations affects its component traits in a pattern that is unique to each cross. Patterns of genetic differentiation among populations of W. smithii provide evidence for a topographically complex “adaptive landscape” as envisioned by Wright in his “shifting balance” theory of evolution. Although we cannot definitively rule out the role of deterministic evolution in the divergence of populations on this landscape, ecological inference and genetic data are more consistent with a stochastic than a deterministic process. At high, limiting larval density, hybrid vigor is enhanced and the influence of epistasis disappears. Thus, under stressful conditions, the advantages to fitness due to hybrid heterozygosity can outweigh the deleterious effects of fragmented gene complexes. These results have important implications for the management of inbred populations. Outbreeding depression assessed in experimental crosses under benign lab, zoo, or farm conditions may not accurately reveal the increased advantages of heterozygosity in suboptimal or marginal conditions likely to be found in nature.

Drought and the organization of tree-hole mosquito communities

SummaryIn southeastern North America (North Florida, USA), the duration, frequency, and timing of drought differentially affect the survivorship of pre-adult tree-hole mosquitoes. Drought affects survivorship both by the direct action of dehydration on developing larvae and pupae and by the indirect modulation of predation. The drought-susceptible species, Toxorhynchites rutilus, Orthopodomyia signifera, and Anopheles barberi co-occur in more permanent holes that are larger, with larger, more vertical openings, lower down in larger trees, and contain darker water with higher conductivity, pH, and tannin-lignin content than the holes occupied by Aedes triseriatus that has drought-resistant eggs and rapid larval development. Ovipositing mosquitoes cue on physical and chemical attributes of tree holes independently of host tree species. These same attributes differ among drought-prone and drought-resistant holes but mosquitoes track these attributes more faithfully than the attributes predict tree-hole stability.

EFFECTS OF POSTGLACIAL RANGE EXPANSION ON ALLOZYME AND QUANTITATIVE GENETIC VARIATION OF THE PITCHER-PLANT MOSQUITO, WYEOMYIA SMITHII

We determined allozyme variability of 34 populations of the pitcher‐plant mosquito, Wyeomyia smithii, from Florida (30°N) to northern Manitoba (54°N) and compared allozyme variability with the additive genetic variance for preadult development time and photoperiodic response determined previously for six populations over a similar range (30–50°N). Phylogenetic analysis of allozymes shows a well‐defined split between Gulf Coast and lowland North Carolina populations, similar to previously observed phylogeographic patterns in a wide variety of taxa. A deeper split in the phylogeny of W. smithii coincides with the location of the maximum extent of the Laurentide Ice Sheet. Furthermore, both average heterozygosity and patterns of isolation‐by‐distance decline in populations north of the former glacial border. It is likely that northern populations are the result of a range expansion that occurred subsequent to the late‐Wisconsin retreat of the Laurentide Ice Sheet and that these populations have not yet reached a drift‐migration equilibrium. The northern decline in allozyme heterozygosity contrasts sharply with the northern increase in additive genetic variance of development time and photoperiodic response found in previous studies. These previous studies also showed that the genetic divergence of populations has involved stochastic variation in the contribution of dominance and epistasis to the genetic architecture underlying demographic traits, including preadult development time, and photoperiodic response. When taken together, the present and prior studies identify the genetic processes underlying the lack of concordance between geographic patterns of allozyme and quantitative genetic variation in natural populations of W. smithii. In the presence of nonadditive genetic variation, isolation and drift can result in opposite patterns of genetic variation for structural genes and quantitative traits.