Heterokairy: a significant form of developmental plasticity?

There is a current surge of research interest in the potential role of developmental plasticity in adaptation and evolution. Here we make a case that some of this research effort should explore the adaptive significance of heterokairy, a specific type of plasticity that describes environmentally driven, altered timing of development within a species. This emphasis seems warranted given the pervasive occurrence of heterochrony, altered developmental timing between species, in evolution. We briefly review studies investigating heterochrony within an adaptive context across animal taxa, including examples that explore links between heterokairy and heterochrony. We then outline how sequence heterokairy could be included within the research agenda for developmental plasticity. We suggest that the study of heterokairy may be particularly pertinent in (i) determining the importance of non-adaptive plasticity, and (ii) embedding concepts from comparative embryology such as developmental modularity and disassociation within a developmental plasticity framework.

Challenges and opportunities in developmental integrative physiology.

This review explores challenges and opportunities in developmental physiology outlined by a symposium at the 2014 American Physiological Society Intersociety Meeting: Comparative Approaches to Grand Challenges in Physiology. Across animal taxa, adverse embryonic/fetal environmental conditions can alter morphological and physiological phenotypes in juveniles or adults, and capacities for developmental plasticity are common phenomena. Human neonates with body sizes at the extremes of perinatal growth are at an increased risk of adult disease, particularly hypertension and cardiovascular disease. There are many rewarding areas of current and future research in comparative developmental physiology. We present key mechanisms, models, and experimental designs that can be used across taxa to investigate patterns in, and implications of, the development of animal phenotypes. Intraspecific variation in the timing of developmental events can be increased through developmental plasticity (heterokairy), and could provide the raw material for selection to produce heterochrony--an evolutionary change in the timing of developmental events. Epigenetics and critical windows research recognizes that in ovo or fetal development represent a vulnerable period in the life history of an animal, when the developing organism may be unable to actively mitigate environmental perturbations. 'Critical windows' are periods of susceptibility or vulnerability to environmental or maternal challenges, periods when recovery from challenge is possible, and periods when the phenotype or epigenome has been altered. Developmental plasticity may allow survival in an altered environment, but it also has possible long-term consequences for the animal. "Catch-up growth" in humans after the critical perinatal window has closed elicits adult obesity and exacerbates a programmed hypertensive phenotype (one of many examples of "fetal programing"). Grand challenges for developmental physiology include integrating variation in developmental timing within and across generations, applying multiple stressor dosages and stressor exposure at different developmental timepoints, assessment of epigenetic and parental influences, developing new animal models and techniques, and assessing and implementing these designs and models in human health and development.

Alarm substance from adult zebrafish alters early embryonic development in offspring.

Alarm substances elicit behavioural responses in a wide range of animals but effects on early embryonic development are virtually unknown. Here we investigated whether skin injury-induced alarm substances caused physiological responses in embryos produced by two Danio species (Danio rerio and Danio albolineatus). Both species showed more rapid physiological development in the presence of alarm substance, although there were subtle differences between them: D. rerio had advanced muscle contraction and heart function, whereas D. albolineatus had advanced heart function only. Hence, alarm cues from injured or dying fish may be of benefit to their offspring, inducing physiological responses and potentially increasing their inclusive fitness.

A copepod life-cycle test and growth model for interpreting the effects of lindane.

A full life-cycle test was performed to measure the effects of lindane (3.2-3,200 microg l(-1)) on the survival, development and reproduction of the freshwater copepod Bryocamptus zschokkei. This copepod survived at relatively high concentrations of lindane compared with other freshwater crustaceans with a 10 day LC50 of 241 microg l(-1) (95% CL of 141-440). 'Equiproportional development', which assumes that each moult stage represents a specific proportion of the total development time, and is not affected by processes that influence metabolism such as temperature and food quality, was used to determine the mode of action of lindane on development in B. zschokkei. Development to adult was significantly longer at 100 microg l(-1) lindane compared with the controls, however, development remained equiproportional regardless of lindane exposure. Increased development times, therefore, are not due to a direct effect of lindane on the moulting process but are due probably to reduced food intake or increased metabolism through the stress imposed by toxicant exposure. Although the survival data suggest that B. zschokkei is relatively tolerant of lindane exposure, reproduction was affected at low lindane concentrations. At 32 microg l(-1) lindane, significantly fewer eggs and viable offspring were produced per female compared with the solvent control. At very low lindane concentrations (3.2 and 10 microg l(-1)), there was a significant increase in the numbers of offspring produced per female compared with the controls and this is interpreted as a hormesis effect. In conclusion, a full life-cycle test demonstrated B. zschokkei is relatively sensitive to lindane compared with other freshwater crustaceans. Incorporating a copepod growth model (equiproportional development) into the life-cycle test design, provided information on the dominant mode of action of the toxicant.

Population structure and dispersal in the Canary Island caddisfly Mesophylax aspersus (Trichoptera, Limnephilidae).

Population genetic structure of the circum-Mediterranean caddisfly Mesophylax aspersus (Trichoptera, Limnephilidae) on the Canary Islands was investigated by studying allozyme variation at nine putative loci in five populations. Genetic variability, population structure and gene flow were compared with data in the literature for continental taxa to assess the effect of isolation of island populations on the genetic structure. Larvae were collected from streams on the islands of Tenerife (one population), La Gomera (two populations in the same catchment) and La Palma (two populations in different catchments). Genetic variability within populations was high relative to that recorded previously for continental Trichoptera, e.g. mean heterozygosity was 0.119--0.336 (0.035--0.15 in continental taxa). Highly significant population structuring was observed (mean F(ST)=0.250), and there was significant within-population structuring (mean F(IS)=0.098). Populations from the same catchment or island were no more similar than populations from different islands, which suggests that occasional long-distance dispersal, both between and within islands, is the predominant influence on the population structure. This dispersal ability has contributed to the colonization of most permanent streams on the Canary Islands by M. aspersus.

Inter- and intraspecific trait compensation of defence mechanisms in freshwater snails.

Trait compensation occurs when mechanically independent adaptations are negatively correlated. Here, we report the first study to demonstrate trait compensation in predator-defence adaptations across several species. Freshwater pulmonate snails exposed experimentally to predation chemical cues from fishes and crushed conspecifics showed clear interspecific differences in their behavioural avoidance responses, which were negatively correlated with shell crush resistance. The type of avoidance response varied between species: thin-shelled species (Lymnaea stagnalis and Physa fontinalis) moved to the water-line or out of the water, while those with thick shells moved under cover or showed a mixed response. There were also intraspecific size-linked differences, with an ontogenetic increase in shell strength accompanied by a decrease in behavioural avoidance. Such trait compensation in response to predation has important implications for interspecific interactions and food-web dynamics.

The relationship between trace metal contamination and stream meiofauna.

The effect of chemical contaminants on freshwater meiofaunal communities is poorly understood and meiofauna rarely form part of environmental impact assessments in fresh waters. The community composition and diversity of meiofauna in streams of southwest England (Cornwall) representing a gradient in trace metal contamination were investigated. Multivariate and univariate statistical techniques were used to correlate community composition, diversity and environmental variables. Meiofaunal communities were very different at sites with high compared with low metal concentrations. Copper, either singly, or in combination with other environmental variables (aluminium, zinc or dissolved organic carbon), was the most important correlate with community composition. Not all meiofaunal species were adversely affected by metals, however, and some taxa, most notably certain cyclopoid copepods, were abundant at high metal concentrations. Moreover, sites with high metal concentrations were not significantly less diverse than sites of low metal concentrations. These data suggest that metal contamination significantly alters the composition of stream meiofaunal assemblages and highlight the importance of including meiofauna in impact studies of fresh waters.