Maternal investment evolves with larger body size and higher diversification rate in sharks and rays

Across vertebrates, live-bearing has evolved at least 150 times from the ancestral state of egg-laying into a diverse array of forms and degrees of prepartum maternal investment. A key question is how this diversity of reproductive modes arose and whether reproductive diversification underlies species diversification? To test these questions, we evaluate the most basal jawed vertebrates, Chondrichthyans, which have one of the greatest ranges of reproductive and ecological diversity among vertebrates. We reconstructed the sequence of reproductive mode evolution across a time-calibrated molecular phylogeny of 610 chondrichthyans. We find that egg-laying is ancestral, and that live-bearing evolved at least seven times. Matrotrophy (i.e. additional maternal contributions) evolved at least 15 times, with evidence of one reversal. In sharks, transitions to live-bearing and matrotrophy are more prevalent in larger-bodied species in the tropics. Further, the evolution of live-bearing is associated with a near-doubling of the diversification rate, but, there is only a small increase in diversification associated with the appearance of matrotrophy. The chondrichthyan diversification and radiation, particularly throughout the shallow tropical shelf seas and oceanic pelagic habitats, appears to be associated with the evolution of live-bearing and the proliferation of a wide range of maternal investment in their developing offspring.

Invasive predators induce plastic and adaptive responses during embryo development in a threatened frog

Invasive predators can strongly affect native populations. If alien predator pressure is strong enough, it can induce anti-predator responses, including phenotypic plasticity of exposed individuals and local adaptations of impacted populations. Furthermore, maternal investment is an additional pathway that could provide resources and improve performance in the presence of alien predators. We investigated the potential responses to an alien predator crayfish (Procambarus clarkii) in a threatened frog (Rana latastei) by combining field observations with laboratory measurements of embryo development rate, to assess the importance of parental investment, origin and exposure to the crayfish cues. We detected a strong variation in parental investment amongst frog populations, but this variation was not related to the invasion status of the site of origin, suggesting that mothers did not modulate parental investment in relation to the presence of alien predators. However, cues of the invasive crayfish elicited plastic responses in clutches and tadpoles development: embryos developed faster when exposed to the predator. Furthermore, embryos from invaded sites reached Gosner’s development stage 25 faster than those from non-invaded sites. This ontogenetic shift can be interpreted as a local adaptation to the alien predator and suggests that frogs are able to recognise the predatory risk. If these plastic responses and local adaptation are effective escape strategies against the invasive predator, they may improve the persistence of native frog populations.

Mothers front-load their investment to the egg stage when helped in a wild cooperative bird

In many cooperative societies, including our own, helpers assist with the post-natal care of breeders' young, and may thereby benefit the post-natal development of offspring. Here we present evidence of a novel mechanism by which such post-natal helping could also have hitherto unexplored beneficial effects on pre-natal development: by lightening post-natal maternal workloads, helpers may allow mothers to increase their pre-natal investment per offspring. We present the findings of a decade-long study of cooperatively breeding white-browed sparrow weaver, Plocepasser mahali, societies. Within each social group, reproduction is monopolized by a dominant breeding pair, and non-breeding helpers assist with nestling feeding. Using a within-mother reaction norm approach to formally identify maternal plasticity, we demonstrate that when mothers have more female helpers they decrease their own post-natal investment per offspring (feed their nestlings at lower rates) but increase their pre-natal investment per offspring (lay larger eggs, which yield heavier hatchlings). That these plastic maternal responses are predicted by female helper number, and not male helper number, implicates the availability of post-natal helping per se as the likely driver (rather than correlated effects of group size), because female helpers feed nestlings at substantially higher rates than males. We term this novel maternal strategy 'maternal front-loading' and hypothesize that the expected availability of post-natal help allows helped mothers to focus maternal investment on the pre-natal phase, to which helpers cannot contribute directly. Such cryptic maternally mediated helper effects on pre-natal development may markedly complicate attempts to identify and quantify the fitness consequences of helping.

Offspring Size, Provisioning and Performance as a Function of Maternal Investment in Direct Developing Whelks

<p>Initial maternal provisioning has pervasive ecological and evolutionary implications for species with direct development, influencing offspring size and energetic content, with subsequent effects on performance, and consequences in fitness for both offspring and mother. Here, using three sympatric marine intertidal direct developing gastropods as model organisms (Cominella virgata, Cominella maculosa and Haustrum scobina) I examined how contrasting strategies of maternal investment influenced development, hatchling size, maternal provisioning and juvenile performance. In these sympatric whelks, duration of intra-capsular development was similar among species (i.e. 10 wk until hatching); nonetheless, differences in provisioning and allocation were observed. Cominella virgata (1 embryo per capsule; ~3 mm shell length [SL]) and C. maculosa (7.7 ± 0.3 embryos per capsule; ~1.5 mm SL) provided their embryos with a jelly-like albumen matrix and all embryos developed. Haustrum scobina encapsulated on average 235 ± 17 embryos per capsule but only ~10 reached the hatching stage (~1.2 mm SL), with the remaining siblings being consumed as nurse embryos, mainly during the first 4 wk of development. Similar chronology in the developmental stages was recognizable among species. Higher growth rates and evident juvenile structures became clear by the second half of development and larval characteristics were less frequently observed. Even after 10 weeks of encapsulation and despite emergent crawling juveniles, some hatchling H. scobina still retained “larval” traits, suggesting that this nurse embryo-based provisioning could result in intracapsular asynchrony of development, and that female of this species would be able to bet-hedge in a higher extent compared with female C. maculosa or C. virgata. Maternal investment in newly laid egg capsules differed among the three study species. The structural lipids phospholipid (PL) and cholesterol (ST) and the energetic lipids aliphatic hydrocarbon (AH), triglycerides (TG), diglycerides (DG) and free fatty acids (FFA) occurred in all three species. Only eggs (and also hatchlings) of the multiencapsulated embryos C. maculosa and H. scobina were provisioned with the energy lipids wax ester (WE) and methyl ester (ME), suggesting an interesting similarity with pelagic larvae of other invertebrates and fish where those lipid classes have also been recorded. Despite differences in hatchling size, the small H. scobina had significantly higher amounts of the energy storage lipid TG compared with C. maculosa and C. virgata, suggesting interesting trade-offs between offspring size and offspring energy resources. H. scobina was the only species that suffered a complete depletion of FFA during development (5th wk), suggesting an additional role of this energetic lipid during the early stages of development. Differences in the amount of lipids among newly laid capsules and siblings within capsules were also detected within species. In both species with multiple embryos per capsule, C. maculosa and H. scobina, these differences were largely explained by variation in TG and PL, enhancing the important role of the major structural (PL) and energy (TG) lipids during the early stages of these whelks, and also providing an integrative approach for evaluating maternally-derived lipids on a perindividual basis in direct developing species with contrasting provisioning and offspring size. Because in direct developers maternal provisioning to the embryos is the primary source of nutrition until offspring enter juvenile life, differences in performance should be closely related with initial provisioning, which in turn may reflect maternal nutritional conditions. Field-based surveys and manipulative experiments in the laboratory showed that different maternal environments (i.e. locations and sites) and contrasting offspring size influenced juvenile performance in different ways for C. virgata and C. maculosa. Despite the large differences in conditions and available resources between the Wellington Harbour and the nearby South Coast, the two locations did not influence the hatchling size of either species, and the most important source of variation was at the smallest scale (i.e. among sites), with substantial variation also occurring within and among females. Between and within species differences in hatching size reflected juvenile performance when fed, regardless of whether subjected to desiccation stress. When starved however, species-specific and size differences in performance were less significant. As has been described for many taxa, large offspring often perform better than small conspecifics; however, because this performance is likely to be context-dependent, understanding the importance of the different scales of variation is crucial for determining how variation in size reflects an organism’s performance. Despite the long recognized role of intra-specific variation in offspring size in mediating subsequent performance, the consequences of inter-specific variation in peroffspring maternal investment for co-occurring taxa have been rarely examined in a predator-prey context. Manipulative experiments in the laboratory with hatchling and juvenile C. virgata and C. maculosa revealed that vulnerability of their early life-stages to common crab predators (i.e. the shore crab Cyclograpsus lavauxi) is highly size-dependent. When predator size was evaluated, small crabs were unable to eat hatchlings of either whelk species. Medium and large shore crabs consumed both prey species; however, hatchlings of C. virgata were less vulnerable to predation by medium crabs than large ones, and C. maculosa were equally vulnerable to both sizes of crabs. In hatchlings of both prey species the shell length and shell thickness increased over time; however, only C. virgata reached a size refuge from predation after two months posthatch. Results showed that vulnerability to predators can be mitigated by larger sizes and thicker shells at hatch; nonetheless, other species-specific traits such as juvenile growth rates, may also play key roles in determining the vulnerability of hatchling and juvenile snails when exposed to shell-crushing predators. Overall, these findings suggest that when defining offspring size, provisioning and performance relationships, many context-dependent scenarios are likely to arise. Therefore examining the early life-history stages of direct developing whelks with contrasting maternal investment under an integrative morphological, physiological and experimental approach, allowed a better understanding of how these complex relationships arises and how mediated the species life-history in terms of offspring size, maternal provisioning and subsequent juvenile performance.</p>

Offspring Size, Provisioning and Performance as a Function of Maternal Investment in Direct Developing Whelks

<p>Initial maternal provisioning has pervasive ecological and evolutionary implications for species with direct development, influencing offspring size and energetic content, with subsequent effects on performance, and consequences in fitness for both offspring and mother. Here, using three sympatric marine intertidal direct developing gastropods as model organisms (Cominella virgata, Cominella maculosa and Haustrum scobina) I examined how contrasting strategies of maternal investment influenced development, hatchling size, maternal provisioning and juvenile performance. In these sympatric whelks, duration of intra-capsular development was similar among species (i.e. 10 wk until hatching); nonetheless, differences in provisioning and allocation were observed. Cominella virgata (1 embryo per capsule; ~3 mm shell length [SL]) and C. maculosa (7.7 ± 0.3 embryos per capsule; ~1.5 mm SL) provided their embryos with a jelly-like albumen matrix and all embryos developed. Haustrum scobina encapsulated on average 235 ± 17 embryos per capsule but only ~10 reached the hatching stage (~1.2 mm SL), with the remaining siblings being consumed as nurse embryos, mainly during the first 4 wk of development. Similar chronology in the developmental stages was recognizable among species. Higher growth rates and evident juvenile structures became clear by the second half of development and larval characteristics were less frequently observed. Even after 10 weeks of encapsulation and despite emergent crawling juveniles, some hatchling H. scobina still retained “larval” traits, suggesting that this nurse embryo-based provisioning could result in intracapsular asynchrony of development, and that female of this species would be able to bet-hedge in a higher extent compared with female C. maculosa or C. virgata. Maternal investment in newly laid egg capsules differed among the three study species. The structural lipids phospholipid (PL) and cholesterol (ST) and the energetic lipids aliphatic hydrocarbon (AH), triglycerides (TG), diglycerides (DG) and free fatty acids (FFA) occurred in all three species. Only eggs (and also hatchlings) of the multiencapsulated embryos C. maculosa and H. scobina were provisioned with the energy lipids wax ester (WE) and methyl ester (ME), suggesting an interesting similarity with pelagic larvae of other invertebrates and fish where those lipid classes have also been recorded. Despite differences in hatchling size, the small H. scobina had significantly higher amounts of the energy storage lipid TG compared with C. maculosa and C. virgata, suggesting interesting trade-offs between offspring size and offspring energy resources. H. scobina was the only species that suffered a complete depletion of FFA during development (5th wk), suggesting an additional role of this energetic lipid during the early stages of development. Differences in the amount of lipids among newly laid capsules and siblings within capsules were also detected within species. In both species with multiple embryos per capsule, C. maculosa and H. scobina, these differences were largely explained by variation in TG and PL, enhancing the important role of the major structural (PL) and energy (TG) lipids during the early stages of these whelks, and also providing an integrative approach for evaluating maternally-derived lipids on a perindividual basis in direct developing species with contrasting provisioning and offspring size. Because in direct developers maternal provisioning to the embryos is the primary source of nutrition until offspring enter juvenile life, differences in performance should be closely related with initial provisioning, which in turn may reflect maternal nutritional conditions. Field-based surveys and manipulative experiments in the laboratory showed that different maternal environments (i.e. locations and sites) and contrasting offspring size influenced juvenile performance in different ways for C. virgata and C. maculosa. Despite the large differences in conditions and available resources between the Wellington Harbour and the nearby South Coast, the two locations did not influence the hatchling size of either species, and the most important source of variation was at the smallest scale (i.e. among sites), with substantial variation also occurring within and among females. Between and within species differences in hatching size reflected juvenile performance when fed, regardless of whether subjected to desiccation stress. When starved however, species-specific and size differences in performance were less significant. As has been described for many taxa, large offspring often perform better than small conspecifics; however, because this performance is likely to be context-dependent, understanding the importance of the different scales of variation is crucial for determining how variation in size reflects an organism’s performance. Despite the long recognized role of intra-specific variation in offspring size in mediating subsequent performance, the consequences of inter-specific variation in peroffspring maternal investment for co-occurring taxa have been rarely examined in a predator-prey context. Manipulative experiments in the laboratory with hatchling and juvenile C. virgata and C. maculosa revealed that vulnerability of their early life-stages to common crab predators (i.e. the shore crab Cyclograpsus lavauxi) is highly size-dependent. When predator size was evaluated, small crabs were unable to eat hatchlings of either whelk species. Medium and large shore crabs consumed both prey species; however, hatchlings of C. virgata were less vulnerable to predation by medium crabs than large ones, and C. maculosa were equally vulnerable to both sizes of crabs. In hatchlings of both prey species the shell length and shell thickness increased over time; however, only C. virgata reached a size refuge from predation after two months posthatch. Results showed that vulnerability to predators can be mitigated by larger sizes and thicker shells at hatch; nonetheless, other species-specific traits such as juvenile growth rates, may also play key roles in determining the vulnerability of hatchling and juvenile snails when exposed to shell-crushing predators. Overall, these findings suggest that when defining offspring size, provisioning and performance relationships, many context-dependent scenarios are likely to arise. Therefore examining the early life-history stages of direct developing whelks with contrasting maternal investment under an integrative morphological, physiological and experimental approach, allowed a better understanding of how these complex relationships arises and how mediated the species life-history in terms of offspring size, maternal provisioning and subsequent juvenile performance.</p>

Reproductive Allocation and Maternal Investment in Intertidal Whelks

<p>Parental investment per offspring is a key life history trait in which offspring size and number combinations are balanced in order to maximise fitness. When food is scarce and energy for reproduction is reduced, changes in reproductive allocation can be expected. These adjustments may go on to influence the growth and survival of the next generation. Trade-offs in reproductive allocation in response to food availability occurred differently in each of the three whelks species of this study. However, each species traded numbers of offspring rather than size of offspring when fed low food. Offspring size was more variable among and within capsules than among food treatments. Capsule size was a plastic trait that varied in response to food treatments in each of the species and varied among populations of the same species. Carry-over effects of maternal nutrition influenced juvenile growth in all three species. However, while juvenile growth was greater when adults were fed high food in two of the species, high adult food suppressed the growth of juveniles of the third species. This may be a mechanism to prevent potential negative consequences of rapid growth. There was no evidence of a maternal effect of mortality in any of the three species. Greater variation in hatchling size occurred in the species in which nurse egg feeding occurred. Nurse egg feeding may be a successful strategy in unpredictable environments where optimal offspring size changes from year to year. Regional differences in reproductive allocation between whelks separated by small distances suggest that populations may be isolated from one another and may need to be managed separately for conservation purposes. This study highlights the influence of maternal nutritional effects on life history and the potential impacts that these may have on population and community structure.</p>

Reproductive Allocation and Maternal Investment in Intertidal Whelks

<p>Parental investment per offspring is a key life history trait in which offspring size and number combinations are balanced in order to maximise fitness. When food is scarce and energy for reproduction is reduced, changes in reproductive allocation can be expected. These adjustments may go on to influence the growth and survival of the next generation. Trade-offs in reproductive allocation in response to food availability occurred differently in each of the three whelks species of this study. However, each species traded numbers of offspring rather than size of offspring when fed low food. Offspring size was more variable among and within capsules than among food treatments. Capsule size was a plastic trait that varied in response to food treatments in each of the species and varied among populations of the same species. Carry-over effects of maternal nutrition influenced juvenile growth in all three species. However, while juvenile growth was greater when adults were fed high food in two of the species, high adult food suppressed the growth of juveniles of the third species. This may be a mechanism to prevent potential negative consequences of rapid growth. There was no evidence of a maternal effect of mortality in any of the three species. Greater variation in hatchling size occurred in the species in which nurse egg feeding occurred. Nurse egg feeding may be a successful strategy in unpredictable environments where optimal offspring size changes from year to year. Regional differences in reproductive allocation between whelks separated by small distances suggest that populations may be isolated from one another and may need to be managed separately for conservation purposes. This study highlights the influence of maternal nutritional effects on life history and the potential impacts that these may have on population and community structure.</p>

Maternal Investment in Adolescent Daughters and Sons

This chapter reflects on maternal investment in adolescent daughters and sons. The focus of maternal investment necessarily changes as a function of the ontological maturity of adolescent sons and daughters. As most sexually mature youth continue to live with parents, mothers’ investments channel youth toward adaptive trajectories given the opportunities and constraints of the local ecology. The nature of childrearing shifts to a greater emphasis on preparing daughters and sons for socio-competitive success; that is, providing resources, particularly those that increase adult knowledge and skills, and protecting offspring from their own adventurousness while learning occurs. Through this focus, mothers facilitate the reproductive success of offspring.