Title: INBREEDING DEPRESSION INCREASES WITH ENVIRONMENTAL STRESS: AN EXPERIMENTAL STUDY AND META-ANALYSIS
Abstract: EvolutionVolume 65, Issue 1 p. 246-258 Free Access INBREEDING DEPRESSION INCREASES WITH ENVIRONMENTAL STRESS: AN EXPERIMENTAL STUDY AND META-ANALYSIS Charles W. Fox, Charles W. Fox Department of Entomology, University of Kentucky, Lexington, Kentucky 40546-0091 E-mail: [email protected] for more papers by this authorDavid H. Reed, David H. Reed Biology Department, University of Louisville, Louisville, Kentucky 40292Search for more papers by this author Charles W. Fox, Charles W. Fox Department of Entomology, University of Kentucky, Lexington, Kentucky 40546-0091 E-mail: [email protected] for more papers by this authorDavid H. Reed, David H. Reed Biology Department, University of Louisville, Louisville, Kentucky 40292Search for more papers by this author First published: 20 August 2010 https://doi.org/10.1111/j.1558-5646.2010.01108.xCitations: 254AboutSectionsPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinked InRedditWechat Abstract Inbreeding–environment interactions occur when inbreeding leads to differential fitness loss in different environments. Inbred individuals are often more sensitive to environmental stress than are outbred individuals, presumably because stress increases the expression of deleterious recessive alleles or cellular safeguards against stress are pushed beyond the organism's physiological limits. We examined inbreeding–environment interactions, along two environmental axes (temperature and rearing host) that differ in the amount of developmental stress they impose, in the seed-feeding beetle Callosobruchus maculatus. We found that inbreeding depression (inbreeding load, L) increased with the stressfulness of the environment, with the magnitude of stress explaining as much as 66% of the variation in inbreeding depression. This relationship between L and developmental stress was not explainable by an increase in phenotypic variation in more stressful environments. To examine the generality of this experimental result, we conducted a meta-analysis of the available data from published studies looking at stress and inbreeding depression. The meta-analysis confirmed that the effect of the environment on inbreeding depression scales linearly with the magnitude of stress; a population suffers one additional lethal equivalent, on average, for each 30% reduction in fitness induced by the stressful environment. Studies using less-stressful environments may lack statistical power to detect the small changes in inbreeding depression. That the magnitude of inbreeding depression scales with the magnitude of the stress applied has numerous repercussions for evolutionary and conservation genetics and may invigorate research aimed at finding the causal mechanism involved in such a relationship. Inbreeding increases genomic homozygosity within individuals and populations. This, in turn, commonly results in a loss of fitness termed inbreeding depression. However, the expression and magnitude of inbreeding depression can be highly sensitive to the environmental conditions under which inbreeding is being measured, because gene expression changes with environmental conditions (genotype–environment interactions; Armbruster and Reed 2005). Genotype–environment interactions have long been considered important to agriculture and animal breeding generally (e.g., Mulder and Bijma 2005), and in evolutionary ecology, because the genetic architecture for traits, and thus evolutionary dynamics, vary with environmental conditions (e.g., Sgrò and Hoffman 2004; Gutteling et al. 2007; Ouborg et al. 2010). Genotype–environment interactions are also important for their potential to maintain genetic diversity (Charlesworth and Hughes 2000). Inbreeding–environment interactions, a special form of genotype–environment interaction, will play a similarly important role whenever individuals and populations differ in their inbreeding levels; in particular inbreeding–environment interactions have been suggested to be crucial for understanding extinction risk (e.g., Reed et al. 2007a; Liao and Reed 2009), the evolution of inbreeding avoidance (Szulkin and Sheldon 2007), and the ability of populations to purge their genetic load when the environment is changing or variable (e.g., Bijlsma et al. 1999; Fox et al. 2008). Inbreeding–environment interactions in which inbreeding depression increases with stress are of special conservation importance. Over the past few centuries, populations of many species of plants and animals have declined and/or become highly fragmented, leading to potentially high levels of inbreeding (Sambatti et al. 2008). This inbreeding due to small population size interacts with anthropogenic environmental changes that tend to produce potentially nonadditive (i.e., worse than expected from considering each effect independently) effects on population dynamics and evolutionary potential. Although studies demonstrating that environmental conditions affect inbreeding depression are ubiquitous, and numerous researchers have posited that inbreeding depression should increase when organisms are under developmental stress, experimental results actually demonstrating that inbreeding depression increases with stress have been inconsistent (e.g., Armbruster and Reed 2005; Marr et al. 2006; Reed et al. 2007a,b; Szulkin and Sheldon 2007; Kristensen et al. 2008; Waller et al. 2008). Many studies have found some relationship between the stressfulness of an environment and inbreeding depression (review in Armbruster and Reed 2005) but many others have failed to find such a relationship (e.g., Fox et al. 2010), leading to a search for alternative explanations to explain variability in inbreeding depression among traits and environments. For example, the phenotypic variability hypothesis of Waller et al. (2008), a form of null model for the relationship between environmental conditions and inbreeding depression, predicts a positive relationship between the shift in inbreeding depression between environments and the difference in the opportunity for selection (CV2) between those environments. Here, we examine the effect of developmental stress, manipulated by varying temperature and diet, on the magnitude of inbreeding depression in the seed-feeding beetle, Callosobruchus maculatus. This beetle exhibits substantial inbreeding depression, and is a model species for previous studies of inbreeding depression and life-history evolution (e.g., Fox et al. 2006; Edvardsson et al. 2008; Bilde et al. 2009). Specifically, we ask whether inbreeding depression increases with increasing developmental stress, with stressfulness of an environment defined as the degree to which mean fitness declines in an environment relative to the best environment. We then review published experimental studies of inbreeding-stress interactions and examine the relationship between degree of stress imposed and the magnitude of inbreeding depression observed. Materials and Methods EXPERIMENTAL STUDY The biology of C. maculatus The life cycle of C. maculatus revolves around their host seeds. Females cement their eggs to the surface of host seeds (Messina 1991). When eggs hatch first-instar larvae burrow into the seed under the egg. Larval development and pupation are completed within a single seed; larvae do not move among seeds and are thus restricted to the seed chosen by their mother. Beetles emerge as reproductively mature adults and require neither food nor water as adults before mating and laying eggs. Here, we use two populations of beetles that have been the focus of a couple of previous inbreeding and life-history studies. The South Indian (SI) population was collected in 1979 from infested pods of mung bean, Vigna radiata (L.) Wilczek, and the closely related black gram, V. mungo (L.) Hepper, in Tirunelveli, India (Mitchell 1991). The Burkina Faso (BF) population was collected in 1989 from infested pods of cowpea, V. unguiculata (L.) Walp., in Ouagadougou, Burkina Faso (Messina 1993). These two populations differ in body size, lifetime fecundity, patterns of egg dispersion, oviposition preference, and adult longevity (Fox et al. 2004a, 2004b; Messina 2004). Both populations were maintained in laboratory growth chambers on seeds of V. radiata (SI) or V. unguiculata (BF) at more than 1000 adults per generation for more than 100 generations (BF) or more than 200 generations (SI) prior to this experiment. Inbreeding depression in C. maculatus Callosobruchus maculatus suffers substantial inbreeding depression throughout development. Eggs produced from inbred matings are less likely to develop, have lower hatch rates, and larvae hatching from these eggs have reduced hatch-to-adult survival. Eggs from full-sibling matings are 17–21% less likely to produce an adult offspring than eggs from outbred matings in these two populations of C. maculatus (Fox et al. 2007). Inbred offspring that survive to adult develop more slowly—larval development time is extended by ∼5% (>1 day) (Tran and Credland 1995; Fox et al. 2007). Inbreeding also negatively affects female fecundity in C. maculatus (Tran and Credland 1995) and its congener C. chinensis (Tanaka 1990, 1993). Experimental design To measure inbreeding depression and the inbreeding load we used a “block” design (Roff 1998; Fig. 1). Blocks were created by randomly pairing two families chosen from an outbred population. From each family, we randomly chose two females and two males to become parents. We crossed these two families creating two inbred and two outbred families per block. The advantage of this design is that it assures that inbred families are created from the same set of alleles as are the outbred families to which they are compared (Fox 2005). Figure 1Open in figure viewerPowerPoint The block design used to measure inbreeding depression. Each block is created by crossing beetles from two unrelated families, creating two outbred matings (reciprocal crosses between the two families) and two inbred matings (crosses between full-siblings within each family). Outbreds and inbreds within each block thus have, on average, the same set of alleles but differ in degree of homozygosity due to the mating treatment. Pairs were confined in a 35-mm Petri dish with 35 seeds of either mung bean, V. radiata, or in a 60-mm petri dish containing 35 seeds of cowpea, V. unguiculata. Each block was assigned to only one host. Dishes were checked for eggs after 12 and 24 h. Eggs laid by females were evenly divided among three temperature treatments, 17°C, 27°C, and 37°C (all ± 0.5), within 12 h of being laid. These temperatures were chosen to include both a low- and high-temperature stress plus an intermediate (benign) temperature. Larval egg-to-adult survival for these two populations is highest at temperatures between 25°C and 30°C (Stillwell et al. 2007). The temperatures were picked to be extreme enough to impose substantial stress on development. Larvae were allowed to develop at one egg per seed (excess eggs were scraped from the seed), one seed per dish, inside a temperature and photoperiod (but not humidity) controlled growth chamber at light:dark 15:9. Dishes were checked twice per day for adult beetles that emerged from a seed. We scored egg and larval survival for all offspring. All of the eggs/larvae were classified to one of four fates; those that failed to develop, developed but did not hatch (a developing larva/embryo was visible inside the clear egg), hatched but did not emerge as an adult, or emerged as an adult. Sample sizes In total, we created 32 blocks (BF population) or 33 blocks (SI population) on each rearing host (64 and 66 blocks total for the BF and SI populations, respectively). Each block consisted of two inbred and two outbred families. From these blocks, we collected a total of 15,664 eggs (∼15.1 eggs per block per inbreeding treatment × rearing host × rearing temperature combination) of which 13,999 developed, 12,308 hatched, and 7,719 survived to adult, from which we have development time data on 7684 offspring. Analyses Blocks are the lowest level of independence in this design and thus block means were used in all analyses. All block means were calculated first by averaging across offspring within a family and then by averaging across families within the block and treatment. Each block contains two means, one for each treatment (inbred and outbred). We used analysis of variance (SAS PROC MIXED; Littell et al. 1996) to test for population, treatment, and interaction effects on the block means for the four measured survival variables, and on inbreeding depression/load (δ and L; see below). We used linear contrasts (CONTRAST statement in PROC MIXED) to test for differences between specific pairs of temperatures. Inbreeding depression, was calculated as the proportional reduction in survival, (Lynch and Walsh 1998). δ was calculated separately for each block (i.e., each group of two inbred and two outbred families), and each estimate of δ was treated as a single independent datapoint. We also calculated the inbreeding load (genetic load, L) for genes affecting larval survival. The genetic load was estimated as (Charlesworth and Charlesworth 1987) where F= 0.25 for our block design. LSurvival was calculated separately for each block. Although we calculated both δ and L for all four survivorship traits that we measured, the two parameters are calculated from the same two values, and are highly correlated. Thus, all statistical analyses are qualitatively identical regardless of whether we use δ or L. We present analyses of L in most places, because our main hypothesis is with regard to the relationship between stress and inbreeding load. However, we also refer to values of δ because it is often more intuitive to interpret proportional reductions in fitness than differences in inbreeding loads. To test whether inbreeding depression was dependent on stressfulness of the environment, we used proportional reduction in survival of outbred offspring during the same period of development, relative to survival in the best temperature/host combination, as our proxy for environmental quality; i.e., stress= 1 −Survivaloutbred(stressful)/Survivaloutbred(benign) within each period of development. This assumes that the environments in which mortality is lowest during a period of development represent the best conditions for that period of development (Armbruster and Reed 2005). We used analysis of covariance to test for a significant relationship between mean L for each host/temperature combination versus stress (model: L= population +stress, with population as a fixed effect and stress as a covariate). [See also our discussion in the next section of the Methods on the intrinsic correlation between these variables]. To test the phenotypic variability hypothesis, we calculated a coefficient of variation (CV) for each survival trait among blocks within each treatment. The hypothesis predicts a positive relationship between the shift in inbreeding depression (or load) between environments and the difference in the opportunity for selection (CV2) between those environments. This is because stress may increase phenotypic variation, enhancing the opportunity for selection and thus inbreeding depression (Waller et al. 2008). We thus tested whether inclusion of CV2 (for each environment) into our model improved the fit of the model over inclusion of stress alone, or explained variation in L better than did the model including only stress (Burnham and Anderson 1998). ANALYSIS OF PUBLISHED STUDIES We then surveyed the literature for papers in which inbreeding was measured in at least two environments that differed in fitness (i.e., one could be considered the stressful environment) and in which the decrease in fitness in the outbred individuals could be ascertained as a measure of stress. The literature search found 58 datapoints, from 33 independently published studies, involving 27 species. A summary of the papers we considered is presented in Table 1, and the data extracted from these are presented in Table S4. They include studies on 11 plant, 13 invertebrate, and three vertebrate species. The stress factors include exposure to insecticides and other noxious or toxic chemicals, nutrient deprivation, temperature and desiccation stress, the effects of competition and parasitism, stressful vs. benign years, and comparisons of natural versus artificial conditions. Table 1. Studies used in our meta-analysis of inbreeding–stress interactions, sorted by author. Estimates of Ldiff and stress used in the analyses are in Table S4 . Citation Species (Order or Family) Taxonomic group Stressor(s) F1 Armbruster et al. (2000) Aedes geniculatus (Diptera) Invertebrate Natural vs. artificial tree holes 0.25–0.375 Bijlsma et al. (1999) Drosophila melanogaster (Diptera) Invertebrate Temperature, ethanol, DDT and crowding 0.402 Bijlsma et al. (2000) Drosophila melanogaster (Diptera) Invertebrate Temperature, ethanol 0.25–0.785 Carr et al. (2003) Mimulus guttatus (Scrophulariaceae) Plant Viral infection 0.50 Chen (1993) Arianta arbustorum (Helicidae) Invertebrate Laboratory vs. field 0.25 Cheptou et al. (2000a) Crepis sancta (Asteraceae) Plant Water (drought) 0.50 Cheptou et al. (2000b) Crepis sancta (Asteraceae) Plant Interspecific competition 0.125–0.25 Dahlgaard et al. (1995) Drosophila buzzatii (Diptera) Invertebrate Heat shock 0.25–0.50 Dahlgaard and Hoffmann (2000) Drosophila melanogaster (Diptera) Invertebrate Heat shock 0.375 Dahlgaard and Loeschcke (1997) Drosophila buzzatii (Diptera) Invertebrate Heat shock 0.25–0.50 Eckert and Barrett (1994) Decodon verticillatus (Lythraceae) Plant Intraspecific competition 0.50 Fowler and Whitlock (2002) Drosophila melanogaster (Diptera) Invertebrate Temperature and density 0.25 Fox et al. (2010) Callosobruchus maculatus (Coleoptera) Invertebrate Temperature 0.25 Haag et al. (2002) Daphnia magna (Daphniidae) Invertebrate Competition 0.50 Haag et al. (2003) Daphnia magna (Daphniidae) Invertebrate Parasitic infection 0.50 Hayes et al. (2005) Cucurbita pepo (Cucurbitaceae) Plant Nitrogen fertilization 0.50 Henry et al. (2003) Physa acuta (Physidae) Invertebrate Laboratory vs. field 0.50 Johnston (1992) Lobelia (two species) (Lobelioideae) Plant Greenhouse vs. field 0.50 Koelewijn (1998) Plantago coronopus (Plantaginaceae) Plant Greenhouse vs. field 0.25–0.875 Kristensen et al. 2003) Drosophila buzzatii (Diptera) Invertebrate Temperature and pesticide 0.25–0.67 Kristensen et al. (2008) Drosophila melanogaster (Diptera) Invertebrate Temperature 0.67 Markert et al. (2010) Americamysis bahia (Mysidae) Invertebrate Diluted seawater 0.125–1.0 Marr et al. (2006) Melospiza melodia (Emberizidae) Vertebrate Natural ecological variation 0.06–0.253 Nowak et al. (2007) Chironomus riparius (Diptera) Invertebrate Cadmium exposure 0.125–0.375 Reed and Bryant (2001) Musca domestica (Diptera) Invertebrate Diet and temperature 0.25 Reed et al. (2002) Drosophila melanogaster (Diptera) Invertebrate Copper sulfate and methanol 0.25–0.83 Reed et al. (2003a) Drosophila melanogaster (Diptera) Invertebrate Copper sulfate and methanol 0.594 Reed et al. (2007b) Rabidosa (two species) (Lycosidae) Invertebrate Natural ecological variation 0.05–0.383 Rowe and Beebee (2005) Bufo calamita (Bufonidae) Vertebrate Natural ecological variation 0.403 Schemske (1983) Costus (three species) (Zingiberaceae) Plant Light availability 0.50 Schmitt and Ehrhardt (1990) Impatiens capensis (Balsaminaceae) Plant Intraspecific competition 0.50 Szulkin and Sheldon (2007) Parus major (Paridae) Vertebrate Natural ecological variation ≥0.1253 Wolfe (1993) Hydrophyllum appendiculatum (Hydrophyllacea) Plant Intraspecific competition 0.50 1Estimated inbreeding coefficient (F) for inbred treatment relative to outbred treatment. F=0.25 for full-sibling matings, F=0.50 for selfing. 2Second chromosome completely homozygous. 3 F based on natural matings, estimated from genetic markers or pedigrees, rather than manipulated by experimenters. For each study, we computed L, the number of haploid lethal equivalents (Armbruster and Reed 2005) under benign and stressful conditions and compared the difference in lethal equivalents (Ldiff=L in the stressful environment minus L in the benign environment) to our proxy for stress, which was the proportional decrease in fitness of outbred individuals in the stressful environment compared to the benign environment (i.e., stress= 1 −Survivaloutbred(stressful)/Survivaloutbred(benign), as in the previous analysis). Specifically, using weighted regression, we test the hypothesis that the difference in genetic load between environments, Ldiff, increases with stress (model: Ldiff=stress) with estimates of Ldiff weighted by the reciprocal of the number of parameter estimates per study. We did not weight estimates of Ldiff by the sample sizes of the individual studies because (1) experimental units varied and were not comparable among studies (individuals, families, blocks, etc.), and (2) our variables stress and Ldiff are functions of fitness and L, respectively, in multiple contexts/treatments (see above), each of which have different sample sizes. Producing a single meaningful value for the sample size or the sample variance for any specific point is not practical. This regression analysis has one obvious problem: both Ldiff and stress include the terms Survivaloutbred(stressful) and Survivaloutbred(benign), and are thus necessarily correlated. However, algebraic rearrangement shows that, ignoring the constant, Ldiff includes the term ln[Survivaloutbred(stressful)/Survivaloutbred(benign)], whereas stress includes −Survivaloutbred(stressful)/Survivaloutbred(benign). The intrinsic correlation is thus negative, which is in the opposite direction of our hypothesis, which predicts a positive relationship. Simulations confirm this; when L varies randomly across environments, the estimated relationship between Ldiff and stress is negative, and when L is defined to increase with stress, the intrinsic correlation reduces (very slightly) the slope of the estimated relationship. When inbreeding depression (δ) is constant across stress levels (a biological possibility, but not a statistical possibility due to sampling error), Ldiff is uncorrelated with stress (because L is a constant). Thus, testing for a positive correlation between Ldiff and stress is a conservative test of the hypothesis that L increases with stress; that is, the nonindependence of the two variables reduces the magnitude of the estimated correlation, and does not inflate the correlation, and thus our estimates of the slope of the relationship underestimate the true slope by a few percent (the effect is small). Results Multiple previous studies have examined the effects of temperature and diet on larval development in these two beetle populations (e.g., Stillwell et al. 2007; Stillwell and Fox 2007, and references therein). Rather than repeating the details of these effects for this particular study, we have placed this information (including statistical analyses and figures) in Supporting information. Mean survival through all four periods of development, for both populations reared on both hosts at three temperatures, is presented in Table 2. Here, we summarize briefly the temperature and host effects necessary to understand our test of the hypothesis that the inbreeding load increases with developmental stress. Table 2. Mean (±SEM) survival during four periods of development (egg development, egg hatch, larval survival, and cumulative probability that an egg produces an adult offspring) for outbred Callosobruchus maculatus reared at three temperatures on two different host species. Means were calculated separately for each family within each block, then averaged across families within blocks, then average across blocks within treatments. N=32 blocks per treatment for the BF population 33 blocks per treatment for the SI population. Temperature/Trait Burkina Faso South India Mung Cowpea Mung Cowpea 17°C Eggs developing1 0.95±0.01 0.89±0.02 0.94±0.02 0.89±0.02 Eggs hatching2 0.94±0.01 0.93±0.01 0.95±0.02 0.91±0.01 Larval survival3 0.80±0.02 0.34±0.03 0.87±0.02 0.17±0.03 Egg→adult4 0.72±0.02 0.29±0.03 0.78±0.02 0.13±0.02 27°C Eggs developing1 0.95±0.01 0.91±0.02 0.93±0.02 0.93±0.02 Eggs hatching2 0.99±0.01 0.98±0.01 0.97±0.02 0.98±0.01 Larval survival3 0.99±0.01 0.87±0.02 0.97±0.02 0.56±0.02 Egg→adult4 0.93±0.01 0.78±0.03 0.88±0.02 0.52±0.02 37°C Eggs developing1 0.91±0.02 0.85±0.02 0.90±0.02 0.85±0.02 Eggs hatching2 0.93±0.01 0.93±0.01 0.91±0.02 0.90±0.02 Larval survival3 0.94±0.01 0.74±0.03 0.87±0.02 0.41±0.03 Egg→adult4 0.79±0.02 0.59±0.03 0.75±0.04 0.33±0.03 1The proportion of eggs producing a visible embryo. 2The proportion of developing eggs that hatch (hatching is defined to have occurred if the larvae begins digging into the seed). 3The proportion of hatched eggs that produce an adult offspring that successfully emerges from the seed; offspring that pupated but failed to emerge from a seed are counted as part of larval mortality. 4The total probability that an egg produces an adult offspring that successfully emerges from the seed. Rearing host had no effect on the proportion of eggs developing or egg hatch, but had a large effect on larval survival and thus on the probability that an egg gave rise to an adult offspring (Table 2; analyses in Supporting information). Mung bean was the better host for both populations of beetles. Temperature did not affect the proportion of eggs that developed, but affected larvae at all subsequent stages of development such that eggs were most likely to give rise to an offspring that survived to adult when reared at 27°C, and least likely to give rise to an adult offspring at 17°C, with 37°C being intermediate (χ21 > 13.3, P < 0.001 for all linear contrasts) (Table 2). There was no overall effect of inbreeding on the proportion of eggs that developed, and the estimate of inbreeding depression (δ) and inbreeding load (L) at this stage did not differ between rearing hosts nor vary among rearing temperatures (Table 3; Fig. 2). However, inbreeding depression and the inbreeding load were significantly >0 at all other stages of development. The clearest pattern, and an important prerequisite for a test between stress and inbreeding depression, is that the inbreeding load varied substantially among the three rearing temperatures and between the two rearing hosts for larval hatch-to adult survival. This resulted in substantial variation among environments in inbreeding depression and the inbreeding load for the proportion of eggs giving rise to an adult offspring (Table 3; Fig. 2). In general, the inbreeding load was greatest at low temperature, and lowest at intermediate temperature (Table 3). However, there were significant population × environment interactions, indicating that the degree to which the inbreeding load varied among environments differed between populations. This included a significant population × temperature × host three-way interaction, which indicated a significant interaction between stressors (temperature and host) for the SI population that did not occur in the BF populations; the effect of rearing host on the inbreeding load was especially large in SI beetles when they were reared at the two extreme temperatures, whereas the effect of host on inbreeding depression was smaller and relatively consistent across temperatures for BF beetles. Table 3. The magnitude of inbreeding depression (δ±SEM) on egg development, egg hatch, larval survival, and the cumulative probability that an egg produces an adult offspring, for outbred and inbred (sib-mated) Callosobruchus maculatus reared on two different host species. δ is the proportional decrease in hatch/survival of inbred relative to outbred beetles. δ was calculated separately for each family within each block, then averaged across families within blocks, then average across blocks within treatments. N=32 blocks per treatment for the BF population, and N=33 blocks per treatment for the SI population. Inbreeding loads are shown in Figure 2. Temperature/Trait Burkina Faso South India Mung Cowpea Mung Cowpea 17°C Eggs developing1 0.08±0.02 0.06±0.03 0.03±0.02 0.02±0.03 Eggs hatching2 0.27±0.03 0.17±0.04 0.21±0.05 0.16±0.03 Larval survival3 0.66±0.03 0.65±0.10 0.45±0.03 0.63±0.13 Egg→adult4 0.77±0.02 0.71±0.09 0.58±0.03 0.65±0.13 27°C Eggs developing1 0.02±0.01 0.03±0.02 0.00±0.03 0.05±0.02 Eggs hatching2 0.10±0.02 0.08±0.02 0.09±0.03 0.06±0.02 Larval survival3 0.09±0.02 0.24±0.03 0.11±0.03 0.20±0.05 E
Publication Year: 2010
Publication Date: 2010-09-15
Language: en
Type: review
Indexed In: ['crossref', 'pubmed']
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Cited By Count: 413
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