Table 1 Definitions

a) Disambiguation

 Paternal effect is a broad term encompassing (i) transgenerational plasticity where the phenotypic change in offspring occurs in response to the paternal environment or phenotype [1], (ii) indirect genetic effects IGEs where alleles expressed in the father affect the development of his offspring [2] and (iii) effects of spontaneous or stochastic variation in non-genetic factors such as epigenetic marks (i.e. variation that is not induced consistently by particular environmental factor). In the current review, we focus on transgenerational plasticity.

b) Meaning of paternal effect across the research fields

 Evolutionary biologists delineate paternal effects most broadly [3]. In this field, a paternal effect reflects the influence of paternal environment or age on offspring traits and can be mediated by paternal care or by factors (such as RNA or proteins) in sperm of seminal fluid. The medical definition usually does not encompass effects transmitted via paternal care [4]. Researchers interested in inheritance of metabolic diseases narrow the definition further into ‘epigenetic programming’ [5] and do not consider age as a part of paternal effects. In terms of the proximate mechanisms, the definitions encompass sperm-borne mechanisms, such as DNA methylation, chromatin alterations and non-coding RNAs [3,4,5,6]. In addition, evolutionary perspective is likely to consider mechanisms acting via ejaculate-borne agents, e.g. RNA and proteins, reviewed by [7].

c) The term ‘paternal effect’ in other contexts

 Identity: the term is sometimes used to account for paternal identity in statistical models, either in a full-factorial experiment [8] or in studies designed to estimate genetic parameters of sires in animal breeding [9].

 Genetics: the term could mean an effect that arises due to the male-specific sex chromosome [10]. The term can denote inheritance of genes through the patriline which exhibits parent-of-origin expression [4], called also ‘epivariation’ [11]. ‘Paternal effect locus’ is a locus whose expression in a male influences the development of his offspring (i.e. an IGE). Recently, it is also referred to as ‘male genetic quality’, related to inbreeding [12].

 Symbionts/parasites: although not commonplace, there is evidence that males may transmit symbionts [13] and parasites to their offspring. For instance, males with Wolbachia cause embryonic lethality [14]. There is also evidence for paternal mitochondria leakage in animals and humans [15]; these phenomena would be classified as male-specific genetic inheritance, yet to our knowledge have so far not been named ‘paternal effect’.

 Assisted reproduction: in assisted reproduction treatment, the term ‘early paternal effect’ refers to failure at the initial stages of the procedure, resulting in zygote malformation, while ‘late paternal effect’ refers to the failure at the stage of implantation [16].

d) Interface of epigenetics and genetics

 Research into paternal effects sheds light on interrelations between different forms of inheritance and their interactions with the environment. First, epigenotype controls the expression of the genotype, while both the genotype and the environment shape the epigenotype [17]. Second, environmentally induced epigenetic processes can promote genetic mutations [18]. Third, factors with mutagenic or cancerogenic effects can also exert epigenetic effects. Exposure to such factors (e.g. smoking) does not allow disentangling the epigenetic effect per se. Finally, classification of effects due to male age is ambiguous. Older males might accumulate effects of lifetime exposure to various environmental [19] and other factors (e.g. exercise). However, older males also have higher numbers of de novo mutations in germline DNA (reviewed, e.g. by [20]) and altered DNA methylation patterns, known as ‘epigenetic clock’ [21], which places age at the interface of genetic and non-genetic factors.