Neriidae is a small, mostly tropical family of true flies (Diptera) with long, stilt-like legs. Many neriid species are strikingly sexually dimorphic in body shape, and the few species that have been observed exhibit remarkable sexual behaviours. Neriid larvae also exhibit interesting behaviours, including the ability to leap when they migrate from the larval feeding substrate to the pupation site. Two neriid species are known in Australia: Telostylinus angusticollis (also known as Derocephalus angusticollis) is native to NSW and southern Queensland. These large flies (up to 2 cm in length) aggregate and breed on rotting bark of Acacia longifolia and a few other trees. Telostylinus lineolatus inhabits tropical north Queensland, where it breeds on rotting fruit, and also occurs on many Pacific islands.
Almost no research had been done on any neriid species when our lab started working on these flies two decades ago. Since then, we have been using the Australian neriid flies in research on nutrition, developmental plasticity, non-genetic inheritance, ageing, and sexual coevolution. The research briefly summarised below encompasses the work of many students and collaborators, especially Margo Adler, Noriyoshi Kawasaki, Elizabeth Cassidy, Eleanor Bath, Alexander Sentinella, Marco Telford, Aidan Runagall-McNaull, Amy Hooper, Foteini Spagopoulou, Erin Macartney, Zachariah Wylde, Kristin Hubakk, Megan Head, Claudia Fricke, Anna Kopps, and Angela Crean.
Our work has shown that T. angusticollis exhibits pronounced sexual dimorphism in the length of the head capsule and antennae, and these secondary sexual traits—used as both weapons and signals—are both absolutely and relatively larger in large males (Bonduriansky 2006). Males with more elongated antennae tend to defeat body size-matched rivals in combat, and tend to mate sooner when paired with females (Fricke et al. 2015). Sexual dimorphism in this species is strikingly condition-dependent: males reared on a nutrient-rich larval diet are considerably larger than females on average and have greatly elongated heads and antennae, while males reared on a nutrient-poor larval diet are smaller than females on average and have a female-like body shape (Bonduriansky 2007). The development of these male secondary sexual traits is especially sensitive to protein concentration in the larval diet, but dietary protein mediates an important trade-off: males reared on high-protein larval diet develop enlarged adult secondary sexual traits but experience reduced juvenile survival (Sentinella et. al. 2013). Larval nutrition also affects developmental stability and integration: larvae reared on nutrient-rich larval diet develop into more symmetrical adults (Bonduriansky 2009), but males have less integrated genitalic traits (Wylde et al. 2020).
Larval nutrition affects adult life history and behaviour as well. Males provided with abundant nutrients as larvae develop faster (Hooper and Bonduriansky 2019). Such males also reach their reproductive peak sooner as adults but then age faster, compared with males reared on a nutrient-poor larval diet (Hooper et al. 2017). This occurs, at least in part, because flies reared on a nutrient-rich larval diet develop more fragile exoskeletons that deteriorate more rapidly with age (Adler et al. 2016). However, restriction of dietary protein at the larval stage tends to shorten adult longevity (Runagall-McNaull et al. 2015). The large, well-armed males that develop on nutrient-rich larval diet are also highly aggressive, often engaging in spectacular battles for control of females and territories near egg-laying sites (Hooper et al. 2017). The effects of larval nutrition on male and female reproductive traits and performance are much stronger and more consistent than the effects of genetic quality (Hooper and Bonduriansky 2022). Indeed, if populations of flies are reared for a single generation on larval diets of differing nutrient concentration (simulating development on distinct host-trees that differ in nutritional profile), the resulting adult populations exhibit very different patterns of reproductive behaviour and sexual competition as well as partial reproductive isolation, providing a potential example of the role of developmental plasticity in adaptive evolution (Hubakk et al. 2024).
Larval nutrition also has interesting effects on male post-copulatory traits and sperm allocation strategy. Males reared on a nutrient-rich larval diet develop relatively larger testes and accessory glands, and produce sperm with a higher tail-beat frequency, compared with males reared on a nutrient-poor larval diet (Macartney et al. 2018). Moreover, labelling of live males’ sperm with rhodamine fluorophores has revealed that males reared on a nutrient-rich larval diet elevate their ejaculate size under conditions of sperm-competition risk, while males reared on nutrient-poor larval diet do not adjust their ejaculate size in this way (Wylde et al. 2020). Nonetheless, regardless of larval nutrition, frequent mating results in reduced male mating rate, perhaps as a strategy to maintain adequate ejaculate size and composition (Macartney et al. 2020).
Notably, larval nutrition not only affects the development and adult phenotype of directly exposed individuals but also the development and fitness of their offspring—an example of nongenetic inheritance. We have found that females reared on a nutrient-rich larval diet produce larger eggs that hatch into larvae that develop faster under nutrient-limited conditions, while males reared on a nutrient-rich larval diet produce offspring that attain a larger adult body size (Bonduriansky and Head 2007). The paternal effect on offspring body size can also be modulated by the social environment (sex ratio) experienced by adult males (Adler et al. 2013). Subsequent experiments based on the ‘nutritional geometry’ framework showed that the paternal effect on offspring body size is mainly dependent on the carbohydrate concentration in the paternal larval diet (Bonduriansky et al. 2016). This work also revealed a maternal effect on offspring growth mediated by protein concentration in the maternal larval diet. Parental larval diet affects offspring viability as well, via opposing maternal and paternal effects: embryo viability is enhanced by protein in the maternal larval diet but reduced by protein in the paternal larval diet (Bonduriansky et al. 2016).
Further work led to the discovery of a novel type of nongenetic effect in T. angusticollis, whereby the effects of male larval diet extend to offspring sired by other males that mate later with the same female. When females were paired sequentially with males reared on different larval diets, paternity analysis based on microsatellite loci (Kopps et al. 2012) showed that the second male sired nearly all of the offspring; yet, the body size of those offspring was affected by the first male’s larval diet (Crean et al. 2013). This effect was not mediated by female differential investment in eggs; rather, it appeared to result from larval diet-regulated factors such as noncoding RNAs transmitted in the seminal fluid and absorbed into developing ovules. We referred to this non-parental nongenetic effect as ‘telegony’, a term coined long ago by August Weismann to refer to hypothetical effects of a female’s first mate on subsequent offspring sired by other males.
The adult diet and other aspects of the adult environment also affect reproductive strategy, survival and performance in T. angusticollis. Restriction of adult dietary protein drastically reduces female reproduction but has more subtle and context-dependent effects on males (Adler et al. 2013). Adult dietary protein can affect offspring fitness as well. Adult males provided with abundant dietary protein sired more viable offspring when young, but the viability of their offspring declined sharply with age as a symptom of accelerated reproductive senescence (Macartney et al. 2017). The adult social environment has important effects on longevity and reproductive strategy. In males, early-life mortality was increased when the adult sex-ratio was male-biased, but ageing rate was increased when the adult sex ratio was female-biased; by contrast, female mortality rate was unaffected by the presence of males, but ageing rate was increased when the adult sex ratio was male-biased (Adler and Bonduriansky 2011). Furthermore, males’ perception of their own dominance status (manipulated by placing males with larger or smaller competitors) affected male cuticular hydrocarbons: males that perceived themselves as subordinate expressed more female-like CHCs, perhaps as a strategy of avoiding damaging fights with stronger rivals (Wylde et al. 2019). The laboratory environment itself has a dramatic effect on life history. A mark-resighting field study showed that T. angusticollis live fivefold longer and males age half as rapidly in the sheltered environment of the lab as they do in the wild, providing a striking example of the environment-dependence of lifespan and ageing (Kawasaki et al. 2008).
Longevity is also strongly affected by parental and grandparental ages at breeding. When T. angusticollis males or females breed at older ages, their offspring and grand-offspring have markedly shorter lifespans (Wylde et al. 2019). These dramatic effects of ancestors’ age at breeding, transmitted through both matrilines and patrilines, likely involve nongenetic inheritance. Although parental age effects have been known for several decades, much more research is required to understand the mechanisms and fitness consequences of such effects.
T. lineolatus is very similar in appearance to T. angusticollis, but also different in some intriguing ways. T. lineolatus is much less sexually dimorphic and developmentally plastic than T. angusticollis (Cassidy et al. 2013). T. angusticollis and T. lineolatus also differ markedly in the shape of the male genitalia (Bath et al. 2012). Males of both species eagerly attempt to mate with heterospecific females, and T. lineolatus males can transfer sperm to T. angusticollis females. Curiously, T. angusticollis males also attempt to copulate with T. lineolatus males. However, the two species cannot produce viable hybrid offspring (Bath et al. 2012).
