Many animals care for and protect their offspring to increase their survival and fitness. Insects care for their young using a range of strategies: some dig underground chambers for their young, whilst others carry their brood around on their own bodies. However, it was unclear when these strategies first evolved in insects.

Now Wang et al. report that they have discovered the earliest fossil evidence of an insect caring for its young, in the form of a female insect preserved with her brood in a specimen of ancient amber. The amber comes from northern Myanmar, where amber deposits are around 95–105 million years old. The fossilised insect is an adult female scale insect with a cluster of around 60 eggs on her abdomen. Six young scale insect nymphs are also preserved in the same piece of amber. Wang et al. named this newly discovered species Wathondara kotejai, after an earth goddess in South-East Asian Buddhist mythology and the late Polish entomologist Jan Koteja.

Most scale insect fossils found to date have been males. Fossilised adult females are scarcer, most likely because female scale insects are wingless and less mobile and therefore less prone to accidental burial. The fossil reported by Wang et al. is therefore a rare find, and it is also sufficiently well preserved to reveal that the female's eggs are contained within a wax-coated egg sac. Today there are many species of scale insects, most of which are parasites of plants and many are economically important pests of trees and shrubs. In living relatives of W. kotejai, females use a similar wax coating to protect themselves and their offspring: young nymphs hatch inside the egg sac and remain there for a few days before emerging into the outside world.

This new fossil provides a unique insight into the anatomy and life cycle of a long-extinct insect; it also demonstrates that brood care in insects is an ancient trait that dates back to at least around 100 million years ago at the height of the age of the dinosaurs.

Brood care is an altruistic trait that evolved to enhance the fitness of offspring at a cost to the parents and represents a breakthrough in the adaptation of organisms to their environment (Tallamy, 1984; Clutton-Brock, 1991; Gilbert and Manica, 2010). Fossil evidence of such an ephemeral behavior is extremely rare, reported mainly in dinosaurs (Meng et al., 2004; Varricchio et al., 2008), ostracods (Siveter et al., 2007, 2014), arachnids (Engel and Grimaldi, 2014), but rarely in insects. Until now only two putative examples in Mesozoic insects have been described based on fossils (Peñalver et al., 2012; Cai et al., 2014). Although phylogenetic analyses suggest some ancient insects evolved brood care (e.g., Korb et al., 2012), only fossils provide unequivocal direct evidence. In this study, we report on an exceptionally preserved insect from mid-Cretaceous Burmese amber, which represents the earliest unequivocal direct evidence of brood care in the insect fossil record and sheds new light on the early evolution of such behavior.

Scale insects (Coccoidea), with about 7800 species, are highly diverse, and most of them are obligatory plant parasites often of economic importance (Ben-Dov et al., 2014). They exhibit many unusual features of morphology, reproduction, and life history and are thus considered as some of the most evolutionarily fascinating organisms amongst insects (Wappler and Ben-Dov, 2008; Hodgson and Hardy, 2013). The female life cycle involves two or three actively feeding instars prior to the adult stage, and adult females are wingless, resembling the immature stages (Gullan and Cook, 2007). In contrast, adult males are delicate, ephemeral insects with simplified wing venation (Hodgson and Hardy, 2013). Scale insects separated from their sister-group, the aphids, at least by the Middle Permian based on the earliest occurrence of Aphidomorpha (Szwedo et al., 2015), with the fossil record probably extending back to the Middle Triassic (trace fossils in Figure 4). However, their fossil record is over-dominated by males entrapped in fossil resins, and fossil adult females are very scarce—probably because they are commonly sedentary or sessile on host plants (Koteja, 2000). To our knowledge, the new fossil is the only Mesozoic record of an adult female, the next oldest being from the late Eocene Baltic amber (Koteja and Żak-Ogaza, 1988).

Figure 4

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Wathondara kotejai is unambiguously referable to Ortheziidae, as evidenced by its general habitus with its body covered with wax plates, ensign-like ovisac, stalked eyes, and well-developed legs (Kozár, 2004). Furthermore, W. kotejai shares two potential synapomorphies with Recent and Tertiary, crown-group Ortheziidae: differentiated apical and subapical setae on the last antennal segment, and trochanter and femur fused (Vea and Grimaldi, 2012). Two Cretaceous genera have been tentatively attributed to Ortheziidae: Burmorthezia Vea and Grimaldi in mid-Cretaceous Burmese amber is considered as an extinct sister group to the crown-group Ortheziidae (Vea and Grimaldi, 2012), while Cretorthezia Koteja and Azar in Early Cretaceous Lebanese amber is probably a stem group of scale insects (Koteja and Azar, 2008; Hodgson and Hardy, 2013) or an extinct group within Ortheziidae (Vea and Grimaldi, 2015). Additionally, a putative female (Cretorthezia sp.) from Burmese amber was tentatively identified as an ortheziid, and its systematic position is still uncertain (Koteja and Azar, 2008; Vea and Grimaldi, 2012). Our new fossil supports the view that crown-group Ortheziidae are present in the mid-Cretaceous.

The seventh, eighth, ninth, and posterior wax lobes of W. kotejai are distinctly extended and cover the ovisac dorsally. The thick wax cover not only protects the adult female but also serves to shelter her eggs and first instars. Extant ortheziid females have a band of pores on the ventral side of the abdomen, which secrete a waxy ovisac. The eggs and hatched nymphs are protected within the ovisac (Figure 3), as in extant ortheziids and monophlebids (Vogelsang and Szklarzewicz, 2001). In extant species, the young nymphs hatch within this ovisac and remain there for a few days until they have acquired a thin covering of wax secretion (visible in our specimens as a slight white pubescence on the fossil nymphs), then crawl out through a split in the wax at the distal end of the ovisac (Gullan and Kosztarab, 1997). Extant first instars are mobile and serve as principle agents for dispersion and seeking out suitable feeding sites (Koteja, 2001). This egg brooding is widely considered to be a primitive form of brood care (e.g., Royle, et al., 2012; Wong et al., 2013; Siveter et al., 2014). Some Early Cretaceous cockroaches have been reported with an ootheca attached (Grimaldi and Engel, 2005, Figure 7.72). However, it is not definitive evidence of egg brooding, because some cockroaches subsequently deposit the ootheca in a suitable crevice. Therefore, W. kotejai provides the earliest unequivocal evidence of brood care in insects.

Brood care is considered to have evolved independently in at least seven insect orders (Wong et al., 2013). This remarkable behavior takes several forms of which the most common are egg brooding and offspring attendance. Scale insects have evolved a variety of methods to protect their eggs and hatched nymphs from unfavorable abiotic conditions and natural enemies. Some extant species (e.g., Diaspididae, some Pseudococcidae) even possess an ovoviviparous form or pseudoplacental viviparity (Gullan and Kosztarab, 1997). In addition to Ortheziidae, ovisacs occur in many other families, for example, Monophlebidae, unrelated Coccidae and many Pseudococcidae, in all of which the secretions of a variety of tubular ducts and disc-pores combine to form the ovisac (Ben-Dov et al., 2014). These various types of ovisacs have evolved convergently to protect their offspring from wet and dry conditions, honeydew contamination, and natural enemies (Gullan and Kosztarab, 1997). Our study demonstrates that these significant behavioral and morphological adaptations, associated with considerable maternal investment, were already well established by the mid-Cretaceous.

Many extant Ortheziidae females feed on roots and fungal mycelia or mosses and lichens (Vea and Grimaldi, 2012) and ‘run about’ in forest litter with the eggs carried in the ovisac attached to their bodies. This is considered to be the most primitive habit in scale insects (Gullan and Kosztarab, 1997; Koteja, 2001), and similar brood care behavior also occurs in other early scale insects, for example, Margarodidae and Matsucoccidae (Koteja, 2001). Therefore, this behavior probably has an early origin and maybe a synapomorphy for scale insects. Flowering plants and ants are thought to be important drivers for radiation of the most diverse advanced group, the neococcoids (Grimaldi and Engel, 2005). However, both factors are absent in the evolutionary history of basal groups of scale insects (Figure 4). Brood care, greatly promoting the survival of offspring (Royle et al., 2012), could therefore have been an important driver for the early radiation of scale insects which occurred during the end of the Jurassic or earliest Cretaceous (Figure 4).

Despite a great taxonomic diversity of extant insects with brood care (Wong et al., 2013), direct evidence of such behavior has been reported only in Cenozoic ambers (Peñalver et al., 2012). The new fossil is unique in providing evidence of ovarian and juvenile developmental stages in a fossil insect. More remarkably, it represents the earliest direct evidence of brood care in insects and highlights the long-term stasis of this behavior in archaeococcoids, extending nearly 100 million years.

Burmese amber (amber from northern Myanmar) harbors the most diverse biota in amber from the Cretaceous, and more than 200 families of arthropods have been reported from this deposit. Amber has been recorded from the Shwebo, Thayetmyo, Pakokku, and Pegu districts in Myanmar. However, the only commercial source is the Hukawng Valley in Tanaing Township, Myitkyina District of Kachin State. The amber under study is from an amber mine located near Noije Bum Village, Tanaing Town (Figure 1 in Kania et al., 2015). Four institutes (Nanjing Institute of Geology and Palaeontology, Lingpoge Amber Museum, Huxuan Amber Museum, and Fushun Amber Institute) have collected more than 100,000 amber pieces from this mine, and each piece commonly contains some insects. All these amber pieces were collected from the ‘amber layer’. These deposits have been investigated and dated in detail by Cruickshank and Ko (2003) and Shi et al. (2012). We tentatively followed the age (98.8 ± 0.6 million years) given by U-Pb dating of zircons from the volcaniclastic matrix of the amber (Shi et al., 2012). However, some evidence (e.g., high degree of roundness of amber, bivalve borings on the surface of the amber) suggests that the amber was probably reworked before being deposited in the volcaniclastic matrix.

The type specimen is currently housed in the Nanjing Institute of Geology and Palaeontology (NIGP), Chinese Academy of Sciences and will eventually be deposited in the Lingpoge Amber Museum in Shanghai (specimen available for study by contacting BW or FX). Photographs were taken using a Zeiss SteREO Discovery V20 microscope system. By merging several photographs of one sample, at different focal planes, a single final photograph was created in which the entire sample was in focus. Blue and green filters were used to improve the contrast between the insect and amber. The figures were prepared with CorelDraw X4 and Adobe Photoshop CS3.

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Author details

1. Bo Wang

   1. State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing, China
   2. Steinmann Institute, University of Bonn, Bonn, Germany

   Contribution

   BW, Conception and design, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article, Contributed unpublished essential data or reagents

   For correspondence

   savantwang@gmail.com

   Competing interests

   The authors declare that no competing interests exist.

2. Fangyuan Xia

   Nanjiao Bieshu 394, Shanghai, China

   Contribution

   FX, Acquisition of data, Analysis and interpretation of data

   Competing interests

   The authors declare that no competing interests exist.

3. Torsten Wappler

   Steinmann Institute, University of Bonn, Bonn, Germany

   Contribution

   TW, Analysis and interpretation of data, Drafting or revising the article

   Competing interests

   The authors declare that no competing interests exist.

4. Ewa Simon

   Department of Zoology, University of Silesia, Katowice, Poland

   Contribution

   ES, Analysis and interpretation of data, Drafting or revising the article

   Competing interests

   The authors declare that no competing interests exist.

5. Haichun Zhang

   State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing, China

   Contribution

   HZ, Acquisition of data, Analysis and interpretation of data

   Competing interests

   The authors declare that no competing interests exist.

6. Edmund A Jarzembowski

   1. State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing, China
   2. Department of Earth Sciences, Natural History Museum, London, United Kingdom

   Contribution

   EAJ, Analysis and interpretation of data, Drafting or revising the article

   Competing interests

   The authors declare that no competing interests exist.

7. Jacek Szwedo

   Department of Invertebrate Zoology and Parasitology, University of Gdańsk, Gdańsk, Poland

   Contribution

   JS, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article

   Competing interests

   The authors declare that no competing interests exist.

   "This ORCID iD identifies the author of this article:" 0000-0002-2796-9538

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