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Fitness and aging in Cardiocondyla obscurior ant queens
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ScienceDirect Fitness and aging in Cardiocondyla obscurior ant queens Jan Oettler and Alexandra Schrempf Easy maintenance, controlled mating and short generation time make Cardiocondyla obscurior an interesting model for social insect aging research. Using this ant we have begun to study the proximate genomic relationship between mating and aging. Although mating in general has a positive effect and results in fertile queens with long life but drastically reduced metabolic rates, mating can also dramatically reduce queen fitness. Here we review a decade of research on factors affecting queen aging rate and contrast these findings with studies on honeybees and solitary aging models. We conclude by giving a brief outlook of what is to be expected from this model in coming years. Address Zoologie/Evolutionsbiologie, Universita¨t Regensburg, D-93040 Regensburg, Germany Corresponding authors: Oettler, Jan ([email protected]) and Schrempf, Alexandra ([email protected])
Current Opinion in Insect Science 2016, 16:58–63 This review comes from a themed issue on Social insects Edited by Judith Korb For a complete overview see the Issue and the Editorial Available online 18th May 2016 http://dx.doi.org/10.1016/j.cois.2016.05.010 2214-5745/# 2016 Elsevier Inc. All rights reserved.
Introduction Social insects have been hailed as models for aging research for two reasons: they exhibit large phenotypic differences in longevity associated with queen and worker castes and queens die at relatively old ages compared to solitary insects [1]. However, despite extensive efforts over the last decade, of which the most significant are covered in this special edition, our understanding of the processes causally involved in social insect aging is still limited. This raises two questions: are we perhaps failing to address the appropriate phenomena and, furthermore, why study social insects at all? First, a queen’s relatively long lifespan is the result of a sheltered life, the absence of potentially life-threatening activities like foraging and a surplus of social care (i.e. help with reproduction and additional somatic care by the extended phenotype, the workers [2]). The worker’s intrinsic short life in contrast most likely evolved as a result of high extrinsic mortality Current Opinion in Insect Science 2016, 16:58–63
because workers are simply more dispensable than queens. Although this is a perfect example of the role of differential gene expression in regulating morph-specific senescence, the study thereof can only elucidate idiosyncrasies specific to social insects. Provocatively speaking such approaches have rather limited general scientific value. Indeed, more interesting for a larger comparative biological framework is the variation in lifespan and aging rates within morphs, not between. Such data are still surprisingly scarce, and mostly come from honeybees. Lifespan variation of queens and workers has been associated with an anti-oxidant effect of the egg-yolk precursor protein vitellogenin [3] which exhibit large differences in fecundity. Under the hypothesis that aging in honey bee workers and queens is regulated by similar pathways, an interesting connection has been made between vitellogenin and variation in aging rate of interior versus exterior workers (e.g. [4]) and between winter bees with excessive fat body protein stores and normal bees, among other factors [5]. Ants are the sister taxon to the Apoidea [6] and it is quite tempting to assume that a ubiquitous protein such as vitellogenin that serves many different functions [7] has been recruited to common aging phenotypes in bees and ants alike. Studies in ants are complicated by the long life of most classic study species, practically limiting what can be done during an average PhD and/or funding period. Probably hindered by this, so far only few studies [8–10,11] have used a comparative approach and addressed findings from solitary models, that is, plasticity of superoxide dismutase expression, telomere length, resistance to oxidative stress and infection, and whole transcriptome changes with age. Here, research on queens of the ant Cardiocondyla obscurior (Figure 1) may be able to make a substantial contribution. This ant shares many of the advantages of classic genetic models because of its short generation time, minute size, and the ease with which it can be mated and maintained under controlled conditions. Although this may well be true for other ants, we are especially thankful for this species’ hardiness to endure the challenges of laboratory life. In C. obscurior, queen life span and reproductive output are positively associated [2,12] and this is not just the result of longlived queens laying eggs over a longer period of time. Rather, queens that produce many eggs per day live considerably longer than queens with lower egg laying rates. This is analogous to the difference between highly www.sciencedirect.com
Aging in Cardiocondyla queens Oettler and Schrempf 59
Figure 1
lifespan). A concerted effort to work out such technical hurdles in as many taxa as possible would drastically increase the significance of the contribution the social insect community as a whole can make to aging research.
Determinants of lifespan in C. obscurior
Current Opinion in Insect Science
Cardiocondyla obscurior queen transporting a worker pupa. Source: Picture by Lukas Schrader.
fecund, long-lived queens and sterile, short-lived workers [1], but extends the phenomenon to variation within the reproductive caste. Another obvious question is whether there is anything to gain from studying non-model organisms that are methodologically inferior and generally less well understood than established genetic models? Flies and nematodes exhibit a decline of fertility with age followed by a post-reproductive period similar to many other Animalia [13]. By contrast, in C. obscurior fecundity does not decline with age indicating a very brief period of reproductive senescence [12]. In this respect the life history of C. obscurior queens differs from those of worms and flies but resembles demographic trajectories of other invertebrate and vertebrate taxa and, interestingly, also those of several plants [13]. Thus, the study of non-models with life history trajectories different from those of established models allows to derive universally valid evolutionary explanations and to uncover common biochemical mechanisms. With regard to methodological hurdles, first genomic resources have been established for representative species of all major clades within the social hymenoptera, including C. obscurior [14]. Recent efforts in this species have also allowed for first glimpses into the genetics underlying ant queen fitness [15,16,17]. Study of causal relationships remains limited as methods for forward genetics are only available for honey bees so far [18]. In taxa such as ants with free larvae (i.e. larvae not reared in enclosed cells) the establishment of methods such as CRISPR-Cas is complicated by the fact that manipulated (injected) eggs need to be returned into the caring social environment and have to be accepted by the nurse workers. Several laboratories (e.g. [19–22]) have promising emerging ant models with specific interesting features with regard to aging (e.g. queen number, extent of polyphenism, fecundity, www.sciencedirect.com
The life history of C. obscurior colonies has been extensively studied over the past 15 years. Average life expectancy of queens is around 6 months, while the sterile workers live 3–4 months. These numbers are proxies, and several environmental and physiological factors affect queen and worker longevity. Mating has a prominent effect and generally increases a queen’s lifespan, independent of her egg laying rate [23]. Overall, fecundity of mated queens is positively correlated with lifespan [12]. In general egg-laying starts 1–2 weeks after mating, increases until queens reach mid-life, plateaus and only decreases in the last 1–2 weeks before the queen’s death [12]. The long life of mated queens seems to be a direct physiological consequence of mating rather than an indirect effect of the social environment, as workers treat queens of varying fecundity equally [23], and queens in isolation live longer after reproductive activation compared to non-reproductive queens [24]. In accordance with this, mating status (virgin vs. mated) and fecundity of queens are not reflected in their cuticular lipid profiles [25], that is, the blend of chemicals that is thought to signal a queen’s fertility [26]. Hence, fecundity signaling may play a less decisive role in C. obscurior compared to other social insects, possibly by reducing the likelihood that the fully sterile workers influence queen lifespan via preferential behaviors. At the same time, another key social trait — queen number — strongly affects aging rates, with several queens together living less long than queens alone or in pairs [27]. In colonies consisting of 8 queens (representing the upper quartile of queen number found in the field (median queen number 5, quartiles 3, 8 [12])), individual queens also have lower individual egg laying rates. Still, overall egg number is higher in multiple queen colonies, and if allowed to grow, these colonies perform significantly better than single or double queen colonies. Thus while social competition has a detrimental effect on individual queens, it is in the interest of highly related workers to increase queen number. Contrasting queen and worker interests regarding allocation of investment into individual (somatic) maintenance and social (reproductive) growth therefore ultimately shape queen lifespan, that is, reproductive output is optimized on the colony rather than the individual level. In addition to mating, life span of individual queens is strongly affected by the quality of the mating partner (Table 1). Experiments in our laboratory are generally conducted with the regularly occurring wingless or socalled ergatoid (literally ‘worker-like’) males. Colonies of Current Opinion in Insect Science 2016, 16:58–63
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Table 1 Cardiocondyla obscurior queen fitness in response to mating (relative to mating with wingless males, the most prevalent condition in nature). Fertility was measured differently across studies and only trends are indicated. Queen type Single queen Single queen Single queen Eight queens Single queen Single queen
Mate type Wingless male Winged male Sterilized wingless male Wingless male Unmated (Virgin) Wingless male, different population, same Wolbachia and Westeberhardia strain)
C. obscurior additionally produce winged males in response to changes in the environment (light, temperature, colony size). This has been interpreted as a dispersal strategy under deteriorating conditions [28] via recruitment of the ancestral male type [29]. Winged males reportedly occur in field populations in Japan [30] and the USA [31], which share a similar genetic background [29]. However, winged males were absent during a yearlong monitoring study conducted in a Brazilian population [32] and occur only rarely under standard laboratory conditions in both lineages (28 8C/23 8C, 12 h/12 h day/night; unpublished data). When their production is induced, winged males leave the nest after several days to disperse; wingless males remain inside the nest for their entire lives, where they mate with freshly eclosing queens. Inbreeding and strict full sib mating for 10 generations leads to colony breakdown in some cases but not to diploid male production [33], which is usually a strong predictor of inbreeding depression in species with single-locus sex determination [34]. In some Cardiocondyla species that have lost the winged male morph completely [29] occasional outbreeding is promoted by polyandry and the exchange of female sexuals between nests [35,36]. Still, many colonies of C. obscurior in the laboratory fare well for years without signs of deleterious inbreeding effects. Despite the hidden exposure to natural selection over many generations of winged males and the large colony-level variation in response thresholds for producing winged males, queens mated to winged males live even longer than queens mated to wingless males [37]. The beneficial effect of mating with the ancestral winged male morph is correlated with a transfer of higher amounts of seminal fluid proteins during copulation [38].
The positive effects of mating By comparing individual whole-body transcriptomes, a first gene expression study of C. obscurior queens with different life expectancies resulting from mating status (virgin, sham-mated, mated) examined mechanistic factors implicated in aging and fecundity [15]. It found that the sets of genes differentially expressed across age and mating groups significantly overlap with genes showing age-related expression changes in female Drosophila melanogaster. Several developmental processes were similarly Current Opinion in Insect Science 2016, 16:58–63
Egg production
Mean lifespan
Reference
Baseline Up Down Down Down Down
26 33 26 20 18 16
[23] [37] [23] [27] [23] [16]
weeks weeks weeks weeks weeks weeks
affected, such as the generation of neurons. Interestingly, gene expression in aged ant queens and flies changed in opposing directions. By contrast to flies, reproductionassociated genes were upregulated and genes associated with metabolic processes and muscle contraction were downregulated in old compared to young ant queens. This suggests that aging in two species with very different life histories is correlated with the same set of conserved pathways but that the regulation thereof is highly plastic. The same study examined the expression patterns of conserved putative aging candidate genes from solitary models, including for instance Neuronal Lazarillo (NLaz, an insect homolog of Apolipoprotein ApoD). Confirming the ubiquitous importance of these ‘aging genes’ across taxa, 21 candidate genes were consistently more expressed in short-lived, unmated queens than in longlived, mated queens and their expression was not correlated with egg-laying rate [15]. Studies in the honeybee suggest that the insulin/insulinlike growth factor signaling pathway (IIS), and the target of rapamycin (TOR) pathway are key players in the proximate regulation of lifespan in social insects [5,39]. This matches the importance of these pathways in solitary organisms [34]. Importantly, upregulation of insulinlike receptor (InR) in older, more fertile Cardiocondyla queens points toward an involvement of IIS but does not suggest a general reversal of the traditional relationship between nutrition and IIS as proposed for the honeybee [3]. Differential expression of a juvenile hormone (JH) binding protein furthermore indicates the involvement of JH, which has been implicated in the regulation of innate immunity [40]. Importantly, lifespan differences were accompanied by differential expression of several conserved genes involved with carbohydrate-metabolism and protein modification and degradation. This indicates that both sham-mated and mated queens invest less into protein turnover despite incurring different metabolic costs from maintenance of viable or unviable sperm and exhibiting different egg-laying rates.
The negative effects of mating In solitary insects, physiological costs of mating are frequently due to conflict between males and females over, www.sciencedirect.com
Aging in Cardiocondyla queens Oettler and Schrempf 61
for example, mating rate, egg production or parental care. In perennial social insects with lifelong pair bonding between males and females however [41], mating is predicted to prove beneficial instead of detrimental with regard to longevity and fecundity even when sperm storage poses a fundamental cost [42]. An exception to this rule is male conflict in polyandrous species which can impose extra costs on queens [38]. Main effectors in the arms race between sexes in solitary organisms are fast evolving male seminal secretions which evoke immune responses in females [43,44] and have profound effects on female lifespan [45,46]. In polyandrous social insects, males may transfer spermatophores or mating plugs composed of seminal fluid proteins to prevent females from re-mating [47,48]. By contrast to the generally positive effect of single mating on queen lifespan, mating with males from a distant population has negative effects. Several studies point to an important role of seminal fluids in determining fitness of the mostly monandrous C. obscurior queens. First, winged males transfer higher amounts of some seminal fluid substances during mating than wingless males [38]. Second, in queens mated to either a male from the same population or to a male from a foreign population (for world-wide distribution see e.g. [17]), origin of the mating partner affected the expression of 13 genes [16]. Of the nine characterized genes overexpressed in queens mated with foreign males, five are also overexpressed after single and/or double mating in Drosophila [49] and four of these code for proteins suggested to be involved in innate immune responses. It has been hypothesized that overexpression of these immune genes after the second but not the first mating in Drosophila females is a response to seminal fluids [49]. Similarly, incompatible seminal fluid proteins may cause immune responses in C. obscurior queens mated to foreign males. Whether undetected variation in endosymbiont strains or immune responses resulting from a mismatch of genitalia in allopatric matings also contribute to hybrid dysfunction remains to be studied.
simultaneously invest more into reproduction matches findings from honeybees. The importance of studying several social insect models is probably best reflected by conflicting results. For example, there is no evidence supporting a prominent role of vitellogenin in C. obscurior aging and future work on more taxa will reveal whether honeybees represent a special case within the social insects. Importantly, in contrast to studies on behavioral performance of aged individuals (e.g. [50]), a senescent physiological phenotype and proximate causes of death have yet to be identified for social insect queens. For instance, do we find signs of neurodegenerative diseases in aged queens, similar to solitary species exhibiting a post-reproductive phase? In addition to the study of female fitness parameters, C. obscurior is an excellent system for comparing lifespan plasticity of male morphs. Although the ancestral winged male morph is as short-lived as any other ant male (the famous ‘flying sperm missiles’), the smaller wingless males can live up to three months and exhibit astonishing virility [51]. Although this variation in lifespan perhaps foremost indicates that senescence is independent of body size, it also demonstrates that this ant with its high levels of phenotypic plasticity allows for conclusive studies of candidate aging pathways. Lastly, a system that allows manipulation of age-structure in entire worker cohorts [52] is optimal for studying how task preference differences and associated energy expenditures translate into worker lifespan variation. Together, investigation of these and other aspects of C. obscurior colony demographics and individual fitness promise to provide insights into the proximate and ultimate causes of aging and senescence.
Acknowledgments The authors thank Eva Schultner, Ju¨rgen Heinze and Judith Korb for comments. This work was supported by the Deutsche Forschungsgemeinschaft (OE 549/2-1; SCHR 1135/5-1).
References and recommended reading Papers of particular interest, published within the period of review, have been highlighted as:
Conclusions Overall, this system, which combines the effects of individual fitness, social environment, sexual selection, and population-specific phenotypic divergence on queen aging, offers great opportunities for a broad range of studies. Extensive data on C. obscurior aging phenotypes and preliminary insights into underlying gene expression differences support findings from both solitary and social species. On the one hand similar genes and pathways regulating metabolism, protein synthesis and proteasome function correlate with aging patterns in C. obscurior and Drosophila. Surprisingly, a high degree of plasticity in the extent and direction of gene expression points to the versatility of gene networks and gene function. On the other hand, the fact that queens reach old ages and www.sciencedirect.com
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Current Opinion in Insect Science 2016, 16:58–63
ScienceDirect Fitness and aging in Cardiocondyla obscurior ant queens Jan Oettler and Alexandra Schrempf Easy maintenance, controlled mating and short generation time make Cardiocondyla obscurior an interesting model for social insect aging research. Using this ant we have begun to study the proximate genomic relationship between mating and aging. Although mating in general has a positive effect and results in fertile queens with long life but drastically reduced metabolic rates, mating can also dramatically reduce queen fitness. Here we review a decade of research on factors affecting queen aging rate and contrast these findings with studies on honeybees and solitary aging models. We conclude by giving a brief outlook of what is to be expected from this model in coming years. Address Zoologie/Evolutionsbiologie, Universita¨t Regensburg, D-93040 Regensburg, Germany Corresponding authors: Oettler, Jan ([email protected]) and Schrempf, Alexandra ([email protected])
Current Opinion in Insect Science 2016, 16:58–63 This review comes from a themed issue on Social insects Edited by Judith Korb For a complete overview see the Issue and the Editorial Available online 18th May 2016 http://dx.doi.org/10.1016/j.cois.2016.05.010 2214-5745/# 2016 Elsevier Inc. All rights reserved.
Introduction Social insects have been hailed as models for aging research for two reasons: they exhibit large phenotypic differences in longevity associated with queen and worker castes and queens die at relatively old ages compared to solitary insects [1]. However, despite extensive efforts over the last decade, of which the most significant are covered in this special edition, our understanding of the processes causally involved in social insect aging is still limited. This raises two questions: are we perhaps failing to address the appropriate phenomena and, furthermore, why study social insects at all? First, a queen’s relatively long lifespan is the result of a sheltered life, the absence of potentially life-threatening activities like foraging and a surplus of social care (i.e. help with reproduction and additional somatic care by the extended phenotype, the workers [2]). The worker’s intrinsic short life in contrast most likely evolved as a result of high extrinsic mortality Current Opinion in Insect Science 2016, 16:58–63
because workers are simply more dispensable than queens. Although this is a perfect example of the role of differential gene expression in regulating morph-specific senescence, the study thereof can only elucidate idiosyncrasies specific to social insects. Provocatively speaking such approaches have rather limited general scientific value. Indeed, more interesting for a larger comparative biological framework is the variation in lifespan and aging rates within morphs, not between. Such data are still surprisingly scarce, and mostly come from honeybees. Lifespan variation of queens and workers has been associated with an anti-oxidant effect of the egg-yolk precursor protein vitellogenin [3] which exhibit large differences in fecundity. Under the hypothesis that aging in honey bee workers and queens is regulated by similar pathways, an interesting connection has been made between vitellogenin and variation in aging rate of interior versus exterior workers (e.g. [4]) and between winter bees with excessive fat body protein stores and normal bees, among other factors [5]. Ants are the sister taxon to the Apoidea [6] and it is quite tempting to assume that a ubiquitous protein such as vitellogenin that serves many different functions [7] has been recruited to common aging phenotypes in bees and ants alike. Studies in ants are complicated by the long life of most classic study species, practically limiting what can be done during an average PhD and/or funding period. Probably hindered by this, so far only few studies [8–10,11] have used a comparative approach and addressed findings from solitary models, that is, plasticity of superoxide dismutase expression, telomere length, resistance to oxidative stress and infection, and whole transcriptome changes with age. Here, research on queens of the ant Cardiocondyla obscurior (Figure 1) may be able to make a substantial contribution. This ant shares many of the advantages of classic genetic models because of its short generation time, minute size, and the ease with which it can be mated and maintained under controlled conditions. Although this may well be true for other ants, we are especially thankful for this species’ hardiness to endure the challenges of laboratory life. In C. obscurior, queen life span and reproductive output are positively associated [2,12] and this is not just the result of longlived queens laying eggs over a longer period of time. Rather, queens that produce many eggs per day live considerably longer than queens with lower egg laying rates. This is analogous to the difference between highly www.sciencedirect.com
Aging in Cardiocondyla queens Oettler and Schrempf 59
Figure 1
lifespan). A concerted effort to work out such technical hurdles in as many taxa as possible would drastically increase the significance of the contribution the social insect community as a whole can make to aging research.
Determinants of lifespan in C. obscurior
Current Opinion in Insect Science
Cardiocondyla obscurior queen transporting a worker pupa. Source: Picture by Lukas Schrader.
fecund, long-lived queens and sterile, short-lived workers [1], but extends the phenomenon to variation within the reproductive caste. Another obvious question is whether there is anything to gain from studying non-model organisms that are methodologically inferior and generally less well understood than established genetic models? Flies and nematodes exhibit a decline of fertility with age followed by a post-reproductive period similar to many other Animalia [13]. By contrast, in C. obscurior fecundity does not decline with age indicating a very brief period of reproductive senescence [12]. In this respect the life history of C. obscurior queens differs from those of worms and flies but resembles demographic trajectories of other invertebrate and vertebrate taxa and, interestingly, also those of several plants [13]. Thus, the study of non-models with life history trajectories different from those of established models allows to derive universally valid evolutionary explanations and to uncover common biochemical mechanisms. With regard to methodological hurdles, first genomic resources have been established for representative species of all major clades within the social hymenoptera, including C. obscurior [14]. Recent efforts in this species have also allowed for first glimpses into the genetics underlying ant queen fitness [15,16,17]. Study of causal relationships remains limited as methods for forward genetics are only available for honey bees so far [18]. In taxa such as ants with free larvae (i.e. larvae not reared in enclosed cells) the establishment of methods such as CRISPR-Cas is complicated by the fact that manipulated (injected) eggs need to be returned into the caring social environment and have to be accepted by the nurse workers. Several laboratories (e.g. [19–22]) have promising emerging ant models with specific interesting features with regard to aging (e.g. queen number, extent of polyphenism, fecundity, www.sciencedirect.com
The life history of C. obscurior colonies has been extensively studied over the past 15 years. Average life expectancy of queens is around 6 months, while the sterile workers live 3–4 months. These numbers are proxies, and several environmental and physiological factors affect queen and worker longevity. Mating has a prominent effect and generally increases a queen’s lifespan, independent of her egg laying rate [23]. Overall, fecundity of mated queens is positively correlated with lifespan [12]. In general egg-laying starts 1–2 weeks after mating, increases until queens reach mid-life, plateaus and only decreases in the last 1–2 weeks before the queen’s death [12]. The long life of mated queens seems to be a direct physiological consequence of mating rather than an indirect effect of the social environment, as workers treat queens of varying fecundity equally [23], and queens in isolation live longer after reproductive activation compared to non-reproductive queens [24]. In accordance with this, mating status (virgin vs. mated) and fecundity of queens are not reflected in their cuticular lipid profiles [25], that is, the blend of chemicals that is thought to signal a queen’s fertility [26]. Hence, fecundity signaling may play a less decisive role in C. obscurior compared to other social insects, possibly by reducing the likelihood that the fully sterile workers influence queen lifespan via preferential behaviors. At the same time, another key social trait — queen number — strongly affects aging rates, with several queens together living less long than queens alone or in pairs [27]. In colonies consisting of 8 queens (representing the upper quartile of queen number found in the field (median queen number 5, quartiles 3, 8 [12])), individual queens also have lower individual egg laying rates. Still, overall egg number is higher in multiple queen colonies, and if allowed to grow, these colonies perform significantly better than single or double queen colonies. Thus while social competition has a detrimental effect on individual queens, it is in the interest of highly related workers to increase queen number. Contrasting queen and worker interests regarding allocation of investment into individual (somatic) maintenance and social (reproductive) growth therefore ultimately shape queen lifespan, that is, reproductive output is optimized on the colony rather than the individual level. In addition to mating, life span of individual queens is strongly affected by the quality of the mating partner (Table 1). Experiments in our laboratory are generally conducted with the regularly occurring wingless or socalled ergatoid (literally ‘worker-like’) males. Colonies of Current Opinion in Insect Science 2016, 16:58–63
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Table 1 Cardiocondyla obscurior queen fitness in response to mating (relative to mating with wingless males, the most prevalent condition in nature). Fertility was measured differently across studies and only trends are indicated. Queen type Single queen Single queen Single queen Eight queens Single queen Single queen
Mate type Wingless male Winged male Sterilized wingless male Wingless male Unmated (Virgin) Wingless male, different population, same Wolbachia and Westeberhardia strain)
C. obscurior additionally produce winged males in response to changes in the environment (light, temperature, colony size). This has been interpreted as a dispersal strategy under deteriorating conditions [28] via recruitment of the ancestral male type [29]. Winged males reportedly occur in field populations in Japan [30] and the USA [31], which share a similar genetic background [29]. However, winged males were absent during a yearlong monitoring study conducted in a Brazilian population [32] and occur only rarely under standard laboratory conditions in both lineages (28 8C/23 8C, 12 h/12 h day/night; unpublished data). When their production is induced, winged males leave the nest after several days to disperse; wingless males remain inside the nest for their entire lives, where they mate with freshly eclosing queens. Inbreeding and strict full sib mating for 10 generations leads to colony breakdown in some cases but not to diploid male production [33], which is usually a strong predictor of inbreeding depression in species with single-locus sex determination [34]. In some Cardiocondyla species that have lost the winged male morph completely [29] occasional outbreeding is promoted by polyandry and the exchange of female sexuals between nests [35,36]. Still, many colonies of C. obscurior in the laboratory fare well for years without signs of deleterious inbreeding effects. Despite the hidden exposure to natural selection over many generations of winged males and the large colony-level variation in response thresholds for producing winged males, queens mated to winged males live even longer than queens mated to wingless males [37]. The beneficial effect of mating with the ancestral winged male morph is correlated with a transfer of higher amounts of seminal fluid proteins during copulation [38].
The positive effects of mating By comparing individual whole-body transcriptomes, a first gene expression study of C. obscurior queens with different life expectancies resulting from mating status (virgin, sham-mated, mated) examined mechanistic factors implicated in aging and fecundity [15]. It found that the sets of genes differentially expressed across age and mating groups significantly overlap with genes showing age-related expression changes in female Drosophila melanogaster. Several developmental processes were similarly Current Opinion in Insect Science 2016, 16:58–63
Egg production
Mean lifespan
Reference
Baseline Up Down Down Down Down
26 33 26 20 18 16
[23] [37] [23] [27] [23] [16]
weeks weeks weeks weeks weeks weeks
affected, such as the generation of neurons. Interestingly, gene expression in aged ant queens and flies changed in opposing directions. By contrast to flies, reproductionassociated genes were upregulated and genes associated with metabolic processes and muscle contraction were downregulated in old compared to young ant queens. This suggests that aging in two species with very different life histories is correlated with the same set of conserved pathways but that the regulation thereof is highly plastic. The same study examined the expression patterns of conserved putative aging candidate genes from solitary models, including for instance Neuronal Lazarillo (NLaz, an insect homolog of Apolipoprotein ApoD). Confirming the ubiquitous importance of these ‘aging genes’ across taxa, 21 candidate genes were consistently more expressed in short-lived, unmated queens than in longlived, mated queens and their expression was not correlated with egg-laying rate [15]. Studies in the honeybee suggest that the insulin/insulinlike growth factor signaling pathway (IIS), and the target of rapamycin (TOR) pathway are key players in the proximate regulation of lifespan in social insects [5,39]. This matches the importance of these pathways in solitary organisms [34]. Importantly, upregulation of insulinlike receptor (InR) in older, more fertile Cardiocondyla queens points toward an involvement of IIS but does not suggest a general reversal of the traditional relationship between nutrition and IIS as proposed for the honeybee [3]. Differential expression of a juvenile hormone (JH) binding protein furthermore indicates the involvement of JH, which has been implicated in the regulation of innate immunity [40]. Importantly, lifespan differences were accompanied by differential expression of several conserved genes involved with carbohydrate-metabolism and protein modification and degradation. This indicates that both sham-mated and mated queens invest less into protein turnover despite incurring different metabolic costs from maintenance of viable or unviable sperm and exhibiting different egg-laying rates.
The negative effects of mating In solitary insects, physiological costs of mating are frequently due to conflict between males and females over, www.sciencedirect.com
Aging in Cardiocondyla queens Oettler and Schrempf 61
for example, mating rate, egg production or parental care. In perennial social insects with lifelong pair bonding between males and females however [41], mating is predicted to prove beneficial instead of detrimental with regard to longevity and fecundity even when sperm storage poses a fundamental cost [42]. An exception to this rule is male conflict in polyandrous species which can impose extra costs on queens [38]. Main effectors in the arms race between sexes in solitary organisms are fast evolving male seminal secretions which evoke immune responses in females [43,44] and have profound effects on female lifespan [45,46]. In polyandrous social insects, males may transfer spermatophores or mating plugs composed of seminal fluid proteins to prevent females from re-mating [47,48]. By contrast to the generally positive effect of single mating on queen lifespan, mating with males from a distant population has negative effects. Several studies point to an important role of seminal fluids in determining fitness of the mostly monandrous C. obscurior queens. First, winged males transfer higher amounts of some seminal fluid substances during mating than wingless males [38]. Second, in queens mated to either a male from the same population or to a male from a foreign population (for world-wide distribution see e.g. [17]), origin of the mating partner affected the expression of 13 genes [16]. Of the nine characterized genes overexpressed in queens mated with foreign males, five are also overexpressed after single and/or double mating in Drosophila [49] and four of these code for proteins suggested to be involved in innate immune responses. It has been hypothesized that overexpression of these immune genes after the second but not the first mating in Drosophila females is a response to seminal fluids [49]. Similarly, incompatible seminal fluid proteins may cause immune responses in C. obscurior queens mated to foreign males. Whether undetected variation in endosymbiont strains or immune responses resulting from a mismatch of genitalia in allopatric matings also contribute to hybrid dysfunction remains to be studied.
simultaneously invest more into reproduction matches findings from honeybees. The importance of studying several social insect models is probably best reflected by conflicting results. For example, there is no evidence supporting a prominent role of vitellogenin in C. obscurior aging and future work on more taxa will reveal whether honeybees represent a special case within the social insects. Importantly, in contrast to studies on behavioral performance of aged individuals (e.g. [50]), a senescent physiological phenotype and proximate causes of death have yet to be identified for social insect queens. For instance, do we find signs of neurodegenerative diseases in aged queens, similar to solitary species exhibiting a post-reproductive phase? In addition to the study of female fitness parameters, C. obscurior is an excellent system for comparing lifespan plasticity of male morphs. Although the ancestral winged male morph is as short-lived as any other ant male (the famous ‘flying sperm missiles’), the smaller wingless males can live up to three months and exhibit astonishing virility [51]. Although this variation in lifespan perhaps foremost indicates that senescence is independent of body size, it also demonstrates that this ant with its high levels of phenotypic plasticity allows for conclusive studies of candidate aging pathways. Lastly, a system that allows manipulation of age-structure in entire worker cohorts [52] is optimal for studying how task preference differences and associated energy expenditures translate into worker lifespan variation. Together, investigation of these and other aspects of C. obscurior colony demographics and individual fitness promise to provide insights into the proximate and ultimate causes of aging and senescence.
Acknowledgments The authors thank Eva Schultner, Ju¨rgen Heinze and Judith Korb for comments. This work was supported by the Deutsche Forschungsgemeinschaft (OE 549/2-1; SCHR 1135/5-1).
References and recommended reading Papers of particular interest, published within the period of review, have been highlighted as:
Conclusions Overall, this system, which combines the effects of individual fitness, social environment, sexual selection, and population-specific phenotypic divergence on queen aging, offers great opportunities for a broad range of studies. Extensive data on C. obscurior aging phenotypes and preliminary insights into underlying gene expression differences support findings from both solitary and social species. On the one hand similar genes and pathways regulating metabolism, protein synthesis and proteasome function correlate with aging patterns in C. obscurior and Drosophila. Surprisingly, a high degree of plasticity in the extent and direction of gene expression points to the versatility of gene networks and gene function. On the other hand, the fact that queens reach old ages and www.sciencedirect.com
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