The ecology and evolution of synchronized reproduction in long-lived plants

Populations of many long-lived plants exhibit spatially synchronized seed production that varies extensively over time, so that seed production in some years is much higher than on average, while in others, it is much lower or absent. This phenomenon termed masting or mast seeding has important consequences for plant reproductive success, ecosystem dynamics and plant–human interactions. Inspired by recent advances in the field, this special issue presents a series of articles that advance the current understanding of the ecology and evolution of masting. To provide a broad overview, we reflect on the state-of-the-art of masting research in terms of underlying proximate mechanisms, ontogeny, adaptations, phylogeny and applications to conservation. While the mechanistic drivers and fitness consequences of masting have received most attention, the evolutionary history, ontogenetic trajectory and applications to plant–human interactions are poorly understood. With increased availability of long-term datasets across broader geographical and taxonomic scales, as well as advances in molecular approaches, we expect that many mysteries of masting will be solved soon. The increased understanding of this global phenomenon will provide the foundation for predictive modelling of seed crops, which will improve our ability to manage forests and agricultural fruit and nut crops in the Anthropocene. This article is part of the theme issue ‘The ecology and evolution of synchronized seed production in plants’.

Do secondary hemiepiphytes exist?

For decades, tropical ecologists distinguished primary (PH) and secondary hemiepiphytes (SH) as two structurally dependent life forms with an epiphytic phase at, respectively, the beginning or the end of their ontogeny. However, the use of these terms has been criticized repeatedly because the term “hemiepiphyte” suggests an unsubstantiated biological similarity in ontogeny, and worse, because it is often used without a qualifier, which makes unambiguous interpretation of the life history of such species impossible. In this paper, we go one step further and ask the question whether an ontogenetic trajectory as described by the term “secondary hemiepiphyte” does exist at all. We show that until now all evidence available for the three families that were traditionally listed as taxa with SHs (Araceae, Cyclanthaceae, Marcgraviaceae) falsifies such claims, but critically discuss reports of possible SHs in other families. In all these cases unambiguous conclusions about the existence of any SH are difficult, but our detailed discussion of potential candidates is meant to provide the basis for focused field studies. Irrespective of the outcome of these studies, we urge researchers to abandon the use of the term SH for the time being: Terminological issues can be discussed once there are data.

Ontogeny of audible squeaks in yellow steppe lemming Eolagurus luteus: trend towards shorter and low-frequency calls is reminiscent of those in ultrasonic vocalization

Background Rodents are thought to be produced their human-audible calls (AUDs, below 20 kHz) with phonation mechanism based on vibration of the vocal folds, whereas their ultrasonic vocalizations (USVs, over 20 kHz) are produced with aerodynamic whistle mechanism. Despite of different production mechanisms, the acoustic parameters (duration and fundamental frequency) of AUDs and USVs change in the same direction along ontogeny in collared lemming Dicrostonyx groenlandicus and fat-tailed gerbil Pachyuromys duprasi. We hypothesize that this unidirectional trend of AUDs and USVs is a common rule in rodents and test whether the AUDs of yellow steppe lemmings Eolagurus luteus would display the same ontogenetic trajectory (towards shorter and low-frequency calls) as their USVs, studied previously in the same laboratory colony. Results We examined for acoustic variables 1200 audible squeaks emitted during 480-s isolation-and-handling procedure by 120 individual yellow steppe lemmings (at 12 age classes from neonates to breeding adults, 10 individuals per age class, up to 10 calls per individual, each individual tested once). We found that the ontogenetic pathway of the audible squeaks, towards shorter and lower frequency calls, was the same as the pathway of USVs revealed during 120-s isolation procedure in a previous study in the same laboratory population. Developmental milestone for the appearance of mature patterns of the squeaks (coinciding with eyes opening at 9–12 days of age), was the same as previously documented for USVs. Similar with ontogeny of USVs, the chevron-like squeaks were prevalent in neonates whereas the squeaks with upward contour were prevalent after the eyes opening. Conclusion This study confirms a hypothesis of common ontogenetic trajectory of call duration and fundamental frequency for AUDs and USVs within species in rodents. This ontogenetic trajectory is not uniform across species.

Ontogenetic shape trajectory of Trichomycterus areolatus varies in response to water velocity environment

Body and head shape among fishes both vary between environments influenced by water velocity and across ontogeny. Although the shape changes associated with variation in average water velocity and ontogeny are well documented, few studies have tested for the interaction between these two variables (i.e., does ontogenetic shape variation differ between velocity environments). We use geometric morphometrics to characterize shape differences in Trichomycterus areolatus, a freshwater catfish found in high and low-velocity environments in Chile. We identify a significant interaction between velocity environment and body size (i.e., ontogeny). Ontogenetic patterns of shape change are consistent with other studies, but velocity environment differentially affects the ontogenetic trajectory of shape development in T. areolatus. Shape change over ontogeny appears more constrained in high-velocity environments compared to low-velocity environments.

Craniofacial development illuminates the evolution of nightbirds (Strisores)

Evolutionary variation in ontogeny played a central role in the origin of the avian skull. However, its influence in subsequent bird evolution is largely unexplored. We assess the links between ontogenetic and evolutionary variation of skull morphology in Strisores (nightbirds). Nightbirds span an exceptional range of ecologies, sizes, life-history traits and craniofacial morphologies constituting an ideal test for evo-devo hypotheses of avian craniofacial evolution. These morphologies include superficially ‘juvenile-like’ broad, flat skulls with short rostra and large orbits in swifts, nightjars and allied lineages, and the elongate, narrow rostra and globular skulls of hummingbirds. Here, we show that nightbird skulls undergo large ontogenetic shape changes that differ strongly from widespread avian patterns. While the superficially juvenile-like skull morphology of many adult nightbirds results from convergent evolution, rather than paedomorphosis, the divergent cranial morphology of hummingbirds originates from an evolutionary reversal to a more typical avian ontogenetic trajectory combined with accelerated ontogenetic shape change. Our findings underscore the evolutionary lability of cranial growth and development in birds, and the underappreciated role of this aspect of phenotypic variability in the macroevolutionary diversification of the amniote skull.

The developmental relationship between teeth and dermal odontodes in the most primitive bony fish Lophosteus

The ontogenetic trajectory of a marginal jawbone of Lophosteus superbus (Late Silurian, 422 Million years old), the phylogenetically most basal stem osteichthyan, visualized by synchrotron microtomography, reveals a developmental relationship between teeth and dermal odontodes that is not evident from the adult morphology. The earliest odontodes are two longitudinal founder ridges formed at the ossification center. Subsequent odontodes that are added lingually to the ridges turn into conical teeth and undergo cyclic replacement, while those added labially achieve a stellate appearance. Stellate odontodes deposited directly on the bony plate are aligned with the alternate files of teeth, whereas new tooth positions are inserted into the files of sequential addition when a gap appears. Successive teeth and overgrowing odontodes show hybrid morphologies around the oral-dermal boundary, suggesting signal cross-communication. We propose that teeth and dermal odontodes are modifications of a single system, regulated and differentiated by the oral and dermal epithelia.

Heterochronic origin of spherical fusulinid foraminifera in the late Paleozoic

Heterochrony describes acceleration, displacement, and/or retardation of descendants’ development events compared with ancestral states and has often been cited as an important process to bring about morphological novelty. It was coined one-and-a-half centuries ago and has been discussed by both paleobiologists and biologists frequently ever since. Many types of fossil organisms preserve aspects of their development histories in their bones or shells that have been used for heterochrony analyses, with body size being used as a developmental age indicator, despite questions being raised regarding this practice. For organisms whose hard structures consist of multiple chambers, or that contain growth lines, age information suggested by these structures independently can facilitate ontogenetic modeling. In this way, relations among size, shape, and age can be established to document patterns of morphological development. Morphological analysis of pseudoschwagerine fusulinids, a fossil foraminifera group that developed a morphologically novel spherical shell, along with their presumptive triticitid ancestors illustrates this approach to heterochrony analysis. Ontogenetic trajectory comparisons of four major pseudoschwagerine genera, as well as those of triticitids, document relations between their shapes, sizes, and developmental ages. A complex of heterochronic patterns, including peramorphic predisplacement, hypermorphosis, and acceleration, characterize pseudoschwagerine development and appear to be responsible for the novel appearance of large, inflated fusiform and spherical tests in these late Paleozoic benthic foraminifera. The morphometric approach employed in this investigation could be applied widely in the quantitative morphological studies of development histories in a variety of other fossil groups.

The asynchronous growth and movement reconstruction of the early molting animals

Epithelium is one of the basic types of animal tissue, in which tissue boundaries are the physical barriers to separate adjust cell clusters. However, tissue boundary in cellular level can hardly found in the fossil records. Here I focus on the growth and movement patterns of the early Ecdysozoa being through quantifying forces in cellular level of the epithelium of two worms from the early Cambrian and Ordovician period. The epithelium cells (might be but not necessarily represent the biological cell) separate adjust body ring of the early Ecdysozoa indicates a precise morphological patterning in cellular level has been established in the early Cambrian. The forces distribution patterns on the body ring suggest the boundary cells are contribute to maintain pressure gradient among rings which are the building blocks of the movement pattern of the worm. The active tension field of the worms plates though ontogenetic trajectory while epithelium cells are in the steady state indicate these molting animals employ asynchronous growth pattern of the epithelium.

The balancing act of Nipponites mirabilis (Nostoceratidae, Ammonoidea): managing hydrostatics during a complex ontogenetic trajectory

Nipponites is a heteromorph ammonoid with a complex and unique morphology that obscures its mode of life and ethology. The seemingly aberrant shell of this Late Cretaceous nostoceratid seems deleterious. However, hydrostatic simulations suggest that this morphology confers several advantages for exploiting a quasi-planktic mode of life. Virtual, 3D models of Nipponites mirabilis were used to compute various hydrostatic properties through 14 ontogenetic stages. At each stage, Nipponites had the capacity for neutral buoyancy and was not restricted to the seafloor. Throughout ontogeny, horizontally facing to upwardly facing soft body orientations were preferred. These orientations were aided by the obliquity of the shell’s ribs, which were parallel to former positions of the aperture during life. Static orientations were somewhat fixed, inferred by stability values that are slightly higher than extant Nautilus. The initial open-whorled, planispiral phase is well suited to horizontal backwards movement with little rocking. Nipponites then deviates from this coiling pattern with a series of alternating U-shaped bends in the shell. This modification allows for proficient rotation about the vertical axis, while possibly maintaining the option for horizontal backwards movement by redirecting its hyponome. These particular hydrostatic properties likely result in a tradeoff between hydrodynamic streamlining, suggesting that Nipponites assumed a low energy lifestyle of slowly pirouetting in search for planktic prey. Each computed hydrostatic property influences the others in some way, suggesting that Nipponites maintained a delicate hydrostatic balancing act throughout its ontogeny in order to facilitate this mode of life.